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Harvey Kliman, MD, PhD

Research Scientist in Obstetrics, Gynecology, and Reproductive Sciences; Director, Reproductive and Placental Research Unit

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Harvey Kliman, MD, PhD

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  • Obstetrics, Gynecology & Reproductive Sciences

    PO Box 208063

    New Haven, CT 06520-8063

    United States

Kliman Laboratory
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Research Summary

Harvey J. Kliman has, in addition to an M.D., a Ph.D. in cellular biochemistry from the University of Chicago. He is currently a Research Scientist in the Department of Obstetrics and Gynecology, Yale University School of Medicine and the Director of the Reproductive and Placental Research Unit with a special interest in infertility and pregnancy complications. He has five areas of research interest:

  1. Implantation research;
  2. Using the placenta to predict autism and other genetic abnormalities;
  3. Elucidating the pathways of serotonin transport and biological action of serotonin in the placenta;
  4. Validating and putting into clinical practice the Estimated Placental Volume (EPV) methodology;
  5. Examining the role serotonin in cancer growth.

Extensive Research Description

Harvey J. Kliman is currently a Research Scientist in the Department of Obstetrics and Gynecology, Yale University School of Medicine and the Director of the Reproductive and Placental Research Unit with a special interest in infertility and pregnancy complications. His five areas of research interest are:

Menstrual Cycle Regulation and Embryo Implantation Research

Menstrual cycle regulation is a critical step in embryo implantation and successfully achieving pregnancy. Since a majority of cases of unexplained infertility may result from implantation failure, there is a need to assess the endometrium accurately for defects that could preclude implantation. Current tools for endometrial evaluation, however, are limited. Based on endometrial expression of cyclin E and p27, we have developed a patented endometrial function test (EFT®) which allows us to evaluate at a molecular level the menstrual cycle regulatory cyclins and to differentiate between normally and abnormally developing, endometrium. Ultimately, we hope this test will prove useful to reproductive endocrinologists in evaluating menstrual cycle irregularities as well as implantation potential. In addition, given that cyclin E and p27 are regulated by estrogen and progesterone, this test may have a role in evaluating the effects of these hormones’ exogenous administration in infertility treatments as well as in other circumstances such as hormone replacement therapy of peri- and post-menopausal women and in clinical conditions that are known to alter or disrupt normal menstrual cycle function. Currently the EFT is used to evaluate patients with infertility and recurrent pregnancy loss. The full potential of these markers will need to be established with prospective, case-controlled multi-center trials that examine different groups of infertility patients to investigate the accuracy of the EFT in predicting pregnancy outcomes in natural cycles, IVF, and donor oocyte patients, work that is currently underway in our laboratory.

Structural Defects in the Placenta Suggest the Presence of Genetic Defects in the Fetus

At the basis of the structure of biological systems are genes that regulate the development of the cells that make up the tissues and organs. We humans start off as a symmetrical ball of cells. Even as our first 50 cells begin to separate themselves into an inner cell mass (which will become the embryo, fetus and, eventually, baby) and the trophoblasts (which will become the placenta), genes are regulating the creation of the developmental axes that will form the basis of the entire organism. Defects in the genes that regulate these processes lead to a wide range of embryonic, fetal and neonatal defects, from minor cosmetic abnormalities, to disasters that terminate pregnancy within a few days to weeks after fertilization. Since the placenta and fetus share the same genome, genetic defects in the fetus are often mirrored in the placenta as abnormal growth patterns. The cellular basis of these placental growth patterns is the dynamic relationship between cytotrophoblast replication and differentiation towards syncytiotrophoblast. We have identified an abnormal growth pattern of the trophoblast layers which appears to be associated with genetic defects in the fetus: trophoblast invaginations. When these deep pits are cut in cross section they appear as trophoblast inclusions. We have shown that compared to the placentas from normal children there is a significantly increased frequency of trophoblast inclusions in cases of known chromosomal diseases, such as trisomy 21, 13 and 18, as well as triploidy (three sets of chromosomes). More recently we have demonstrated an increased frequency of inclusions in cases of subtle genetic diseases, including autism.

Pathway of serotonin and biological action in human trophoblasts

Serotonin (5-hydroxytryptamine; 5-HT) is essential to intrauterine development, but its source is debated. Using immunocytochemistry we have localized 5-HT; its biosynthetic enzyme (tryptophan hydroxylase 1, TPH1); an importer (serotonin transporter, 5-HTT/SERT/SLC6A); other transporters (P-glycoprotein 1 [P-gp/ABCB1], OCT3/SLC22A3 and gap junction connexin-43); and the 5-HT degradative enzyme (monoamine oxidase A, MAOA) in sections of placentas. We found in humans that 5-HT was faintly stained only in first trimester trophoblasts, while TPH1 was not seen at any stage. SERT was expressed in syncytiotrophoblasts and, more strongly, in cytotrophoblasts. MAOA was prominent in syncytiotrophoblasts, OCT3 and gap junctions were stained in cytotrophoblasts, and P-gp was present at the apical surfaces of both epithelia. 5-HT added to cultured placental explants accumulated in the trophoblast epithelium and reached the villus core vessels. Trophoblast uptake was blocked by the SERT inhibitor, escitalopram (Lexapro). Inhibition of gap junctions with heptanol prevented the accumulation of 5-HT in cytotrophoblasts, while blocking OCT3 with decynium-22 and P-gp with mitotane both led to its accumulation in cytotrophoblasts. Reducing 5-HT destruction by inhibiting MAOA with clorgyline increased the accumulation of 5-HT throughout the villus. In the mouse fetus, intravascular platelets stained prominently for 5-HT at day 13.5, while the placenta and yolk sac endoderm were both negative. TPH1 was not detected, but SERT was prominent in these mouse tissues. We conclude from these studies that serotonin is conveyed from the maternal blood stream through syncytiotrophoblasts, cytotrophoblasts and the villus core to the fetus through a physiological pathway that involves at least SERT, gap junctions, P-gp, OCT3, and MAOA. We are currently studying the intracellular pathways and binding partners of serotonin in human placental trophoblasts.

Novel method of determining placental volume reduces the risk of intrauterine growth restriction (IUGR) and intrauterine fetal demise (IUFD)

We have developed a mathematical solution to accurately estimate intrauterine placental volume. Care givers of pregnant women currently only track the growth of the fetus without any insight into the growth of the placenta, despite its importance in prenatal development. The placenta is the critical organ responsible for both respiratory and nutritional support of the fetus. In situations where the placenta is significantly small or large for gestational age, a care giver may not have any warning that the fetus is compromised or near death until it is too late. Fetal complications due to placental abnormalities occur in as many as 20% of pregnancies. Clinical intervention is possible with early detection. This invention allows for assessment of in utero placental volume using three basic measurements: width, height and thickness of the placenta. There are no alternative Currently there are no simple, reliable or convenient methods to determine the volume and/or weight of a placenta prior to delivery available today. We propose to use this method to generate normative data on a large population of pregnant women which can be used to automatically flag abnormal placental size. Such normative data will form the basis for the generation of tables which can be incorporated into future ultrasound devices. This will empower future caregivers to identify and intervene in cases where an IUFD would have been the first indication of any problems. This method will create a “placenta tank” gauge where none has existed.This compromises a health care provider’s ability to assess the state of a pregnancy since the placenta is the critical organ responsible for both respiratory and nutritional support of the fetus. Currently care givers of pregnant women only track the growth of the fetus without any insight into the growth the placenta. In situations where the placenta is significantly small or large for gestational age a care giver may not have any warning that the fetus is compromised or near death until it is too late. This invention teaches the use of mathematical equations to estimate the in utero placental volume using three basic measurements: width, height and thickness of the placenta.

Role of Serotonin in cancer proliferation

Serotonin (5-hydroxytryptamine; 5-HT) is a multifunctional molecule. It is found in the gut in specialized cells that interdigitate with the epithelial cells, functioning as a very primitive neuroendocrine system. It is also found in platelets where it is released at locations of tissue damage, participating in wound healing and tissue repair by inducing localized cell proliferation. In addition to serotonin’s role in wound healing some evidence exists that 5-HT may play a role in tissue regeneration and cancer. We are currently examining the role of serotonin in cancer growth and testing ways to kill cancer cells by inhibiting serotonin synthesis.

Coauthors

Research Interests

Autistic Disorder; Endometrium; Female Urogenital Diseases and Pregnancy Complications; Infertility; Placenta; Pregnancy; Reproductive Medicine

Public Health Interests

Reproduction; Child/Adolescent Health; Perinatal/Prenatal Health

Research Images

Placenta predicts the brain
Abnormal folds in the baby's placenta (left) mirror changes in the brain (right), signaling autism risk at birth. See Walker CK, Anderson KW, Milano KM, Ye S, Tancredi DJ, Pessah IN, Hertz-Picciotto I, Kliman HJ. (2013) Trophoblast Inclusions are Significantly Increased in the Placentas of Children in Families at Risk for Autism, Biological Psychiatry, http://dx.doi.org/10.1016/j.biopsych.2013.03.006

Selected Publications

  • Clinical approach to recurrent implantation failure: evidence-based evaluation of the endometrium.Kliman HJ, Frankfurter D. Clinical approach to recurrent implantation failure: evidence-based evaluation of the endometrium. Fertility And Sterility 2019, 111: 618-628. PMID: 30929719, DOI: 10.1016/j.fertnstert.2019.02.011.
  • An experimental test of the ovulatory homolog model of female orgasm.Pavlicev M, Zupan AM, Barry A, Walters S, Milano KM, Kliman HJ, Wagner GP. An experimental test of the ovulatory homolog model of female orgasm. Proceedings Of The National Academy Of Sciences Of The United States Of America 2019, 116: 20267-20273. PMID: 31570579, PMCID: PMC6789565, DOI: 10.1073/pnas.1910295116.
  • Estimated Placental Volume and Gestational Age.Isakov KMM, Emerson JW, Campbell KH, Galerneau F, Anders AM, Lee YK, Subramanyam P, Roberts AE, Kliman HJ. Estimated Placental Volume and Gestational Age. American Journal Of Perinatology 2018, 35: 748-757. PMID: 29281842, DOI: 10.1055/s-0037-1615285.
  • Pathway of Maternal Serotonin to the Human Embryo and Fetus.Kliman HJ, Quaratella SB, Setaro AC, Siegman EC, Subha ZT, Tal R, Milano KM, Steck TL. Pathway of Maternal Serotonin to the Human Embryo and Fetus. Endocrinology 2018, 159: 1609-1629. PMID: 29381782, DOI: 10.1210/en.2017-03025.
  • Luteal start vaginal micronized progesterone improves pregnancy success in women with recurrent pregnancy loss.Stephenson MD, McQueen D, Winter M, Kliman HJ. Luteal start vaginal micronized progesterone improves pregnancy success in women with recurrent pregnancy loss. Fertility And Sterility 2017, 107: 684-690.e2. PMID: 28081870, DOI: 10.1016/j.fertnstert.2016.11.029.
  • Placental 11 β-hydroxysteroid dehydrogenase type 2 (11β-HSD2) expression very early during human pregnancy.Salvante KG, Milano K, Kliman HJ, Nepomnaschy PA. Placental 11 β-hydroxysteroid dehydrogenase type 2 (11β-HSD2) expression very early during human pregnancy. Journal Of Developmental Origins Of Health And Disease 2017, 8: 149-154. PMID: 28112069, DOI: 10.1017/S2040174416000611.
  • Utilizing two-dimensional ultrasound to develop normative curves for estimated placental volume.Arleo EK, Troiano RN, da Silva R, Greenbaum D, Kliman HJ. Utilizing two-dimensional ultrasound to develop normative curves for estimated placental volume. American Journal Of Perinatology 2014, 31: 683-8. PMID: 24108663, DOI: 10.1055/s-0033-1357265.
  • Comment on "the placenta harbors a unique microbiome".Kliman HJ. Comment on "the placenta harbors a unique microbiome". Science Translational Medicine 2014, 6: 254le4. PMID: 25232175, DOI: 10.1126/scitranslmed.3009864.
  • Trophoblast inclusions are significantly increased in the placentas of children in families at risk for autism.Walker CK, Anderson KW, Milano KM, Ye S, Tancredi DJ, Pessah IN, Hertz-Picciotto I, Kliman HJ. Trophoblast inclusions are significantly increased in the placentas of children in families at risk for autism. Biological Psychiatry 2013, 74: 204-11. PMID: 23623455, PMCID: PMC3755347, DOI: 10.1016/j.biopsych.2013.03.006.
  • Placental protein 13 and decidual zones of necrosis: an immunologic diversion that may be linked to preeclampsia.Kliman HJ, Sammar M, Grimpel YI, Lynch SK, Milano KM, Pick E, Bejar J, Arad A, Lee JJ, Meiri H, Gonen R. Placental protein 13 and decidual zones of necrosis: an immunologic diversion that may be linked to preeclampsia. Reproductive Sciences (Thousand Oaks, Calif.) 2012, 19: 16-30. PMID: 21989657, DOI: 10.1177/1933719111424445.
  • Determination of placental weight using two-dimensional sonography and volumetric mathematic modeling.Azpurua H, Funai EF, Coraluzzi LM, Doherty LF, Sasson IE, Kliman M, Kliman HJ. Determination of placental weight using two-dimensional sonography and volumetric mathematic modeling. American Journal Of Perinatology 2010, 27: 151-5. PMID: 19653142, DOI: 10.1055/s-0029-1234034.
  • Timing of fetal meconium absorption by amnionic macrophages.Funai EF, Labowsky AT, Drewes CE, Kliman HJ. Timing of fetal meconium absorption by amnionic macrophages. American Journal Of Perinatology 2009, 26: 93-7. PMID: 19031358, DOI: 10.1055/s-0028-1103028.
  • IFPA meeting 2008 workshops report.Lash GE, Ansari T, Bischof P, Burton GJ, Chamley L, Crocker I, Dantzer V, Desoye G, Drewlo S, Fazleabas A, Jansson T, Keating S, Kliman HJ, Lang I, Mayhew T, Meiri H, Miller RK, Nelson DM, Pfarrer C, Roberts C, Sammar M, Sharma S, Shiverick K, Strunk D, Turner MA, Huppertz B. IFPA meeting 2008 workshops report. Placenta 2009, 30 Suppl A: S4-14. PMID: 19084270, PMCID: PMC2668143, DOI: 10.1016/j.placenta.2008.11.014.
  • The fetus, not the mother, elicits maternal immunologic rejection: lessons from discordant dizygotic twin placentas.Yusuf K, Kliman HJ. The fetus, not the mother, elicits maternal immunologic rejection: lessons from discordant dizygotic twin placentas. Journal Of Perinatal Medicine 2008, 36: 291-6. PMID: 18598117, DOI: 10.1515/JPM.2008.054.
  • Placental trophoblast inclusions in autism spectrum disorder.Anderson GM, Jacobs-Stannard A, Chawarska K, Volkmar FR, Kliman HJ. Placental trophoblast inclusions in autism spectrum disorder. Biological Psychiatry 2007, 61: 487-91. PMID: 16806106, DOI: 10.1016/j.biopsych.2006.03.068.
  • Reference weights for placentas delivered before the 28th week of gestation.Hecht JL, Kliman HJ, Allred EN, Pflueger SM, Chang CH, Doss BJ, Roberts D, Livasy CA, Bhan I, Zambrano E, Ross DW, Senagore P, Husain AN, Leviton A. Reference weights for placentas delivered before the 28th week of gestation. Placenta 2007, 28: 987-90. PMID: 17573110, DOI: 10.1016/j.placenta.2007.04.009.
  • Mouse ascites Golgi mucin expression abnormalities in natural cycle endometrial biopsies predict subsequent in vitro fertilization-embryo transfer (IVF-ET) failure in patients with previous IVF-ET failures.Catalanotti JS, Spandorfer SD, Barmat LI, Rosenwaks Z, McSweet JC, Kliman HJ. Mouse ascites Golgi mucin expression abnormalities in natural cycle endometrial biopsies predict subsequent in vitro fertilization-embryo transfer (IVF-ET) failure in patients with previous IVF-ET failures. Fertility And Sterility 2006, 85: 255-8. PMID: 16412771, DOI: 10.1016/j.fertnstert.2005.06.060.
  • Optimization of endometrial preparation results in a normal endometrial function test (EFT) and good reproductive outcome in donor ovum recipients.Kliman HJ, Honig S, Walls D, Luna M, McSweet JC, Copperman AB. Optimization of endometrial preparation results in a normal endometrial function test (EFT) and good reproductive outcome in donor ovum recipients. Journal Of Assisted Reproduction And Genetics 2006, 23: 299-303. PMID: 16983518, DOI: 10.1007/s10815-006-9061-1.
  • The placenta may predict the baby.Kliman HJ, Segel L. The placenta may predict the baby. Journal Of Theoretical Biology 2003, 225: 143-5. PMID: 14559066, DOI: 10.1016/s0022-5193(03)00248-0.
  • Improved endometrial assessment using cyclin E and p27.Dubowy RL, Feinberg RF, Keefe DL, Doncel GF, Williams SC, McSweet JC, Kliman HJ. Improved endometrial assessment using cyclin E and p27. Fertility And Sterility 2003, 80: 146-56. PMID: 12849817, DOI: 10.1016/s0015-0282(03)00573-9.
  • Sexual activity, orgasm and tampon use are associated with a decreased risk for endometriosis.Meaddough EL, Olive DL, Gallup P, Perlin M, Kliman HJ. Sexual activity, orgasm and tampon use are associated with a decreased risk for endometriosis. Gynecologic And Obstetric Investigation 2002, 53: 163-9. PMID: 12053101, DOI: 10.1159/000058368.
  • Mouse ascites golgi (MAG) mucin expression and regulation by progesterone in the rat uterus.Schwartz LB, Naftolin F, Lyttle CR, Penzias AS, Meaddough EL, Kliman HJ. Mouse ascites golgi (MAG) mucin expression and regulation by progesterone in the rat uterus. Journal Of The Society For Gynecologic Investigation 2001, 8: 216-23. PMID: 11525897, DOI: 10.1016/s1071-5576(01)00115-0.
  • Endometrial dating and determination of the window of implantation in healthy fertile women.Acosta AA, Elberger L, Borghi M, Calamera JC, Chemes H, Doncel GF, Kliman H, Lema B, Lustig L, Papier S. Endometrial dating and determination of the window of implantation in healthy fertile women. Fertility And Sterility 2000, 73: 788-98. PMID: 10731542, DOI: 10.1016/s0015-0282(99)00605-6.
  • Uteroplacental blood flow. The story of decidualization, menstruation, and trophoblast invasion.Kliman HJ. Uteroplacental blood flow. The story of decidualization, menstruation, and trophoblast invasion. The American Journal Of Pathology 2000, 157: 1759-68. PMID: 11106547, PMCID: PMC1885765, DOI: 10.1016/S0002-9440(10)64813-4.
  • The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation.Nachtigall MJ, Kliman HJ, Feinberg RF, Olive DL, Engin O, Arici A. The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. The Journal Of Clinical Endocrinology And Metabolism 1996, 81: 801-6. PMID: 8636307, DOI: 10.1210/jcem.81.2.8636307.
  • Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in the human fallopian tube.Keltz MD, Attar E, Buradagunta S, Olive DL, Kliman HJ, Arici A. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in the human fallopian tube. American Journal Of Obstetrics And Gynecology 1996, 175: 1611-9. PMID: 8987949, DOI: 10.1016/s0002-9378(96)70114-x.
  • Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells.Arici A, Tazuke SI, Attar E, Kliman HJ, Olive DL. Interleukin-8 concentration in peritoneal fluid of patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells. Molecular Human Reproduction 1996, 2: 40-5. PMID: 9238656, DOI: 10.1093/molehr/2.1.40.
  • The efficacy of the placental biopsy.Kliman HJ, Perrotta PL, Jones DC. The efficacy of the placental biopsy. American Journal Of Obstetrics And Gynecology 1995, 173: 1084-8. PMID: 7485298, DOI: 10.1016/0002-9378(95)91331-9.
  • A mucin-like glycoprotein identified by MAG (mouse ascites Golgi) antibodies. Menstrual cycle-dependent localization in human endometrium.Kliman HJ, Feinberg RF, Schwartz LB, Feinman MA, Lavi E, Meaddough EL. A mucin-like glycoprotein identified by MAG (mouse ascites Golgi) antibodies. Menstrual cycle-dependent localization in human endometrium. The American Journal Of Pathology 1995, 146: 166-81. PMID: 7531946, PMCID: PMC1870765.
  • Monoclonal antibody X18A4 identifies an oncofetal fibronectin epitope distinct from the FDC-6 binding site.Feinberg RF, Kliman HJ, Bedian V, Monzon-Bordonaba F, Menzin AW, Wang CL. Monoclonal antibody X18A4 identifies an oncofetal fibronectin epitope distinct from the FDC-6 binding site. American Journal Of Obstetrics And Gynecology 1995, 172: 1526-36. PMID: 7538728, DOI: 10.1016/0002-9378(95)90491-3.
  • Endosalpingiosis found at laparoscopy for chronic pelvic pain.Keltz MD, Kliman HJ, Arici AM, Olive DL. Endosalpingiosis found at laparoscopy for chronic pelvic pain. Fertility And Sterility 1995, 64: 482-5. PMID: 7641898.
  • First-trimester endocervical irrigation: feasibility of obtaining trophoblast cells for prenatal diagnosis.Bahado-Singh RO, Kliman H, Feng TY, Hobbins J, Copel JA, Mahoney MJ. First-trimester endocervical irrigation: feasibility of obtaining trophoblast cells for prenatal diagnosis. Obstetrics And Gynecology 1995, 85: 461-4. PMID: 7862393, DOI: 10.1016/0029-7844(94)00416-b.
  • Color Doppler flow patterns and flow velocity waveforms of the intraplacental fetal circulation in growth-retarded fetuses.Rotmensch S, Liberati M, Luo JS, Kliman HJ, Gollin Y, Bellati U, Hobbins JC, Copel JA. Color Doppler flow patterns and flow velocity waveforms of the intraplacental fetal circulation in growth-retarded fetuses. American Journal Of Obstetrics And Gynecology 1994, 171: 1257-64. PMID: 7977530, DOI: 10.1016/0002-9378(94)90143-0.
  • Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro: implications for trophoblast implantation in vivo.Feinberg RF, Kliman HJ, Wang CL. Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro: implications for trophoblast implantation in vivo. The Journal Of Clinical Endocrinology And Metabolism 1994, 78: 1241-8. PMID: 8175984, DOI: 10.1210/jcem.78.5.8175984.
  • The placenta revealed.Kliman HJ. The placenta revealed. The American Journal Of Pathology 1993, 143: 332-6. PMID: 8342590, PMCID: PMC1887036.
  • Fetal fibronectin and preterm labor.Feinberg RF, Kliman HJ. Fetal fibronectin and preterm labor. The New England Journal Of Medicine 1992, 326: 708; author reply 709. PMID: 1736115, DOI: 10.1056/NEJM199203053261013.
  • Preeclampsia, trisomy 13, and the placental bed.Feinberg RF, Kliman HJ, Cohen AW. Preeclampsia, trisomy 13, and the placental bed. Obstetrics And Gynecology 1991, 78: 505-8. PMID: 1870809.
  • Fetal akinesia deformation sequence (Pena-Shokeir phenotype) associated with acquired intrauterine brain damage.Lavi E, Montone KT, Rorke LB, Kliman HJ. Fetal akinesia deformation sequence (Pena-Shokeir phenotype) associated with acquired intrauterine brain damage. Neurology 1991, 41: 1467-8. PMID: 1891100, DOI: 10.1212/wnl.41.9.1467.
  • Is oncofetal fibronectin a trophoblast glue for human implantation?Feinberg RF, Kliman HJ, Lockwood CJ. Is oncofetal fibronectin a trophoblast glue for human implantation? The American Journal Of Pathology 1991, 138: 537-43. PMID: 2000933, PMCID: PMC1886265.
  • In vitro systems for the study of human trophoblast implantation.Coutifaris C, Babalola GO, Abisogun AO, Kao LC, Chin U, Vadillo-Ortega F, Osheroff J, Kliman HJ, Strauss JF. In vitro systems for the study of human trophoblast implantation. Annals Of The New York Academy Of Sciences 1991, 622: 191-201. PMID: 2064180, DOI: 10.1111/j.1749-6632.1991.tb37862.x.
  • Human trophoblast-endometrial interactions in an in vitro suspension culture system.Kliman HJ, Feinberg RF, Haimowitz JE. Human trophoblast-endometrial interactions in an in vitro suspension culture system. Placenta 1990, 11: 349-67. PMID: 2235916, DOI: 10.1016/s0143-4004(05)80226-7.
  • Aggregation of dispersed human cytotrophoblastic cells: lessons relevant to the morphogenesis of the placenta.Babalola GO, Coutifaris C, Soto EA, Kliman HJ, Shuman H, Strauss JF. Aggregation of dispersed human cytotrophoblastic cells: lessons relevant to the morphogenesis of the placenta. Developmental Biology 1990, 137: 100-8. PMID: 2295358, DOI: 10.1016/0012-1606(90)90011-7.
  • Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity.Kliman HJ, Feinberg RF. Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proceedings Of The National Academy Of Sciences Of The United States Of America 1990, 87: 3057-61. PMID: 2326266, PMCID: PMC53833, DOI: 10.1073/pnas.87.8.3057.
  • Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts.Feinberg RF, Kao LC, Haimowitz JE, Queenan JT, Wun TC, Strauss JF, Kliman HJ. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts. Laboratory Investigation; A Journal Of Technical Methods And Pathology 1989, 61: 20-6. PMID: 2473276.
  • Control of the steroidogenic machinery of the human trophoblast by cyclic AMP.Nulsen JC, Silavin SL, Kao LC, Ringler GE, Kliman HJ, Strauss JF. Control of the steroidogenic machinery of the human trophoblast by cyclic AMP. Journal Of Reproduction And Fertility. Supplement 1989, 37: 147-53. PMID: 2553955.
  • The human trophoblast: homotypic and heterotypic cell-cell interactions.Kliman HJ, Coutifaris C, Babalola GO, Soto EA, Kao LC, Queenan JT, Feinberg RF, Strauss JF. The human trophoblast: homotypic and heterotypic cell-cell interactions. Progress In Clinical And Biological Research 1989, 294: 425-34. PMID: 2726976.
  • The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation.Kao LC, Caltabiano S, Wu S, Strauss JF, Kliman HJ. The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Developmental Biology 1988, 130: 693-702. PMID: 2848742, DOI: 10.1016/0012-1606(88)90361-2.
  • Biosynthesis and turnover of a 34-kDa protein growth factor in human cytotrophoblasts.Roy-Choudhury S, Sen-Majumdar A, Murthy U, Mishra VS, Kliman HJ, Nestler JE, Strauss JF, Das M. Biosynthesis and turnover of a 34-kDa protein growth factor in human cytotrophoblasts. European Journal Of Biochemistry / FEBS 1988, 172: 777-83. PMID: 3350024, DOI: 10.1111/j.1432-1033.1988.tb13957.x.
  • 8-Bromo-adenosine 3',5'-monophosphate regulates expression of chorionic gonadotropin and fibronectin in human cytotrophoblasts.Ulloa-Aguirre A, August AM, Golos TG, Kao LC, Sakuragi N, Kliman HJ, Strauss JF. 8-Bromo-adenosine 3',5'-monophosphate regulates expression of chorionic gonadotropin and fibronectin in human cytotrophoblasts. The Journal Of Clinical Endocrinology And Metabolism 1987, 64: 1002-9. PMID: 2435752, DOI: 10.1210/jcem-64-5-1002.
  • HLA antigen expression and induction by gamma-interferon in cultured human trophoblasts.Feinman MA, Kliman HJ, Main EK. HLA antigen expression and induction by gamma-interferon in cultured human trophoblasts. American Journal Of Obstetrics And Gynecology 1987, 157: 1429-34. PMID: 3122576, DOI: 10.1016/s0002-9378(87)80238-7.
  • Gonadotropins and cyclic adenosine 3',5'-monophosphate (cAMP) alter the morphology of cultured human granulosa cells.Soto EA, Kliman HJ, Strauss JF, Paavola LG. Gonadotropins and cyclic adenosine 3',5'-monophosphate (cAMP) alter the morphology of cultured human granulosa cells. Biology Of Reproduction 1986, 34: 559-69. PMID: 3008869, DOI: 10.1095/biolreprod34.3.559.
  • Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae.Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986, 118: 1567-82. PMID: 3512258, DOI: 10.1210/endo-118-4-1567.
  • 8-Bromo-3',5'-adenosine monophosphate stimulates the endocrine activity of human cytotrophoblasts in culture.Feinman MA, Kliman HJ, Caltabiano S, Strauss JF. 8-Bromo-3',5'-adenosine monophosphate stimulates the endocrine activity of human cytotrophoblasts in culture. The Journal Of Clinical Endocrinology And Metabolism 1986, 63: 1211-7. PMID: 3531221, DOI: 10.1210/jcem-63-5-1211.
  • Glyceraldehyde-3-phosphate dehydrogenase of rat erythrocytes has no membrane component.Ballas SK, Kliman HJ, Smith ED. Glyceraldehyde-3-phosphate dehydrogenase of rat erythrocytes has no membrane component. Biochimica Et Biophysica Acta 1985, 831: 142-9. PMID: 4041465, DOI: 10.1016/0167-4838(85)90161-x.
  • Association of glyceraldehyde-3-phosphate dehydrogenase with the human red cell membrane. A kinetic analysis.Kliman HJ, Steck TL. Association of glyceraldehyde-3-phosphate dehydrogenase with the human red cell membrane. A kinetic analysis. The Journal Of Biological Chemistry 1980, 255: 6314-21. PMID: 7391020.
  • Trophoblast inclusions in the human placenta: Identification, characterization, quantification, and interrelations of subtypes.Kliman HJ, Firestein MR, Hofmann KM, Milano KM, Holzer PH, Brink LT, Odendaal HJ, Fifer WP. Trophoblast inclusions in the human placenta: Identification, characterization, quantification, and interrelations of subtypes. Placenta 2021, 103: 172-176. PMID: 33152642, PMCID: PMC8448462, DOI: 10.1016/j.placenta.2020.10.014.
  • SARS-CoV-2 infection in pregnancy is associated with robust inflammatory response at the maternal-fetal interface.Lu-Culligan A, Chavan AR, Vijayakumar P, Irshaid L, Courchaine EM, Milano KM, Tang Z, Pope SD, Song E, Vogels CBF, Lu-Culligan WJ, Campbell KH, Casanovas-Massana A, Bermejo S, Toothaker JM, Lee HJ, Liu F, Schulz W, Fournier J, Muenker MC, Moore AJ, Konnikova L, Neugebauer KM, Ring A, Grubaugh ND, Ko AI, Morotti R, Guller S, Kliman HJ, Iwasaki A, Farhadian SF. SARS-CoV-2 infection in pregnancy is associated with robust inflammatory response at the maternal-fetal interface. MedRxiv : The Preprint Server For Health Sciences 2021 PMID: 33532791, PMCID: PMC7852242, DOI: 10.1101/2021.01.25.21250452.
  • Genetics, not the uterine environment, drive the formation of trophoblast inclusions: Insights from a twin study.Katz J, Holzer PH, Kliman HJ. Genetics, not the uterine environment, drive the formation of trophoblast inclusions: Insights from a twin study. Placenta 2021, 114: 133-138. PMID: 33941390, DOI: 10.1016/j.placenta.2021.04.010.
  • Loss of Cxcr4 in Endometriosis Reduces Proliferation and Lesion Number while Increasing Intraepithelial Lymphocyte Infiltration.Tal A, Tal R, Kliman HJ, Taylor HS. Loss of Cxcr4 in Endometriosis Reduces Proliferation and Lesion Number while Increasing Intraepithelial Lymphocyte Infiltration. The American Journal Of Pathology 2021, 191: 1292-1302. PMID: 33964217, PMCID: PMC8261475, DOI: 10.1016/j.ajpath.2021.04.011.
  • Maternal respiratory SARS-CoV-2 infection in pregnancy is associated with a robust inflammatory response at the maternal-fetal interface.Lu-Culligan A, Chavan AR, Vijayakumar P, Irshaid L, Courchaine EM, Milano KM, Tang Z, Pope SD, Song E, Vogels CBF, Lu-Culligan WJ, Campbell KH, Casanovas-Massana A, Bermejo S, Toothaker JM, Lee HJ, Liu F, Schulz W, Fournier J, Muenker MC, Moore AJ, Konnikova L, Neugebauer KM, Ring A, Grubaugh ND, Ko AI, Morotti R, Guller S, Kliman HJ, Iwasaki A, Farhadian SF. Maternal respiratory SARS-CoV-2 infection in pregnancy is associated with a robust inflammatory response at the maternal-fetal interface. Med (New York, N.Y.) 2021, 2: 591-610.e10. PMID: 33969332, PMCID: PMC8084634, DOI: 10.1016/j.medj.2021.04.016.
  • Noyes, Hertig, and Rock revisited.Kliman HJ. Noyes, Hertig, and Rock revisited. F&S Reports 2020, 1: 2-4. PMID: 34223203, PMCID: PMC8244307, DOI: 10.1016/j.xfre.2020.04.004.
  • Bone marrow-derived progenitor cells contribute to remodeling of the postpartum uterus.Tal R, Kisa J, Abuwala N, Kliman HJ, Shaikh S, Chen AY, Lyu F, Taylor HS. Bone marrow-derived progenitor cells contribute to remodeling of the postpartum uterus. Stem Cells (Dayton, Ohio) 2021, 39: 1489-1505. PMID: 34224633, DOI: 10.1002/stem.3431.
  • YAP1 nuclear efflux and transcriptional reprograming follow membrane diminution upon VSV-G-induced cell fusion.Feliciano D, Ott CM, Espinosa-Medina I, Weigel AV, Benedetti L, Milano KM, Tang Z, Lee T, Kliman HJ, Guller SM, Lippincott-Schwartz J. YAP1 nuclear efflux and transcriptional reprograming follow membrane diminution upon VSV-G-induced cell fusion. Nature Communications 2021, 12: 4502. PMID: 34301937, PMCID: PMC8302681, DOI: 10.1038/s41467-021-24708-2.
  • Trophoblast inclusions and adverse birth outcomes.Firestein MR, Kliman HJ, Sania A, Brink LT, Holzer PH, Hofmann KM, Milano KM, Pini N, Shuffrey LC, Odendaal HJ, Fifer WP. Trophoblast inclusions and adverse birth outcomes. PloS One 2022, 17: e0264733. PMID: 35231069, PMCID: PMC8887719, DOI: 10.1371/journal.pone.0264733.
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