Skip to main content

Advertisement

SpringerLink
Log in

Impact of Immune Deficiency on Remodeling of Maternal Resistance Vasculature 4 Weeks Postpartum in Mice

  • Original Article
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Pregnancy manifests changes in the vascular and immune systems that persist postpartum (PP), have important implications for future pregnancies, and may modify responses to cardiovascular stress in late life. The association between immune and vascular function and the generation or progression of cardiovascular disease beg the question of whether altered immunity modifies pregnancy-induced changes in the vasculature. Our objective was to compare changes in the function and remodeling of systemic resistance vessels 4 weeks PP in normal C57BL/6 (B6), and immunodeficient mice recombinase 1-deficient/B6 (Rag1−/−). Immune deficiency did not change the responsiveness to acetylcholine (ACh) and phenylephrine at baseline but decreased arterial dis-tensibility and increased stiffness PP. Adoptive transfer of CD8 T cells into Rag1−/− mice decreased the response to ACh while increasing distensibility and wall thickness. When compared to PP Rag1−/−, vessels from PP CD4-deficient mice, which have B cells and CD8 T cells, but no CD4 cells, show increased distensibility and decreased responsiveness to ACh in a pattern similar to that seen in Rag1−/− given CD8 T cells prior to mating. These studies suggest a key role for T cell, particularly CD8 T cell, associated factors in the PP remodeling of maternal resistance vessels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Meah VL, Cockcroft JR, Backx K, Shave RI, Stöhr EJ. Cardiac output and related haemodynamics during pregnancy: a series of meta-analyses. Heart. 2016;102(7):518–526.

    Article  CAS  PubMed  Google Scholar 

  2. Bernstein IM, Ziegler W, Badger GJ. Plasma volume expansion in early pregnancy. Obstet Gynecol. 2001;97(5 pt 1):669-672.

    Google Scholar 

  3. Wedel Jones C, Mandala M, Barron C, Bernstein I, Osol G. Mechanisms underlying maternal venous adaptation in pregnancy. Reprod Sci. 2009;16(6):596–604.

    Article  PubMed  CAS  Google Scholar 

  4. Magness RR, Parker CR Jr, Rosenfeld CR. Systemic and uterine responses to chronic infusion of estradiol-17 beta. Am J Physiol. 1993;265(5 pt 1):E690–E698.

    CAS  PubMed  Google Scholar 

  5. Osol G, Mandala M. Maternal uterine vascular remodeling during pregnancy. Physiol. 2009;24:58-71.

    Article  Google Scholar 

  6. Cooke CLM, Davidge ST. Pregnancy-induced alterations of vascular function in mouse mesenteric and uterine arteries. Biol Reprod. 2003;68(3):1072–1077.

    Article  CAS  PubMed  Google Scholar 

  7. Gokina NI, Kuzina OY, Vance AM. Augmented EDHF signaling in rat uteroplacental vasculature during late pregnancy. Am J Physiol Heart Circ Physiol. 2010;299(5):H1642–H1652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tropea T, De Francesco EM, Rigiracciolo D, et al. Pregnancy augments G protein estrogen receptor (GPER) induced vasodila-tion in rat uterine arteries via the nitric oxide—cGMP signaling pathway. PLoS One. 2015;10(11):e0141997.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Morris EA, Hale SA, Badger GJ, Magness RR, Bernstein IM. Pregnancy induces persistent changes in vascular compliance in primiparous women. Am J Obstet Gynecol. 2015;212(5):633. e631–636.

    Article  Google Scholar 

  10. Yuan LJ, Xue D, Duan YY, Cao TS, Zhou N. Maternal carotid remodeling and increased carotid arterial stiffness in normal late-gestational pregnancy as assessed by radio-frequency ultrasound technique. BMC Pregnancy Childbirth. 2013;13:122.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Limon-Miranda S, Salazar-Enriquez DG, Muniz J, et al. Pregnancy differentially regulates the collagens types I and III in left ventricle from rat heart. Biomed Res Int. 2014;2014:ID984785: 1–5.

    Article  CAS  Google Scholar 

  12. Hilgers RH, Bergaya S, Schiffers PM, et al. Uterine artery structural and functional changes during pregnancy in tissue kallikrein-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23(10):1826–1832.

    Article  CAS  PubMed  Google Scholar 

  13. Clapp J. 3rd, Capeless E. Cardiovascular function before, during, and after the first and subsequent pregnancies. Am J Cardiol. 1997;80(11):1469–1473.

    Article  PubMed  Google Scholar 

  14. Euser AG, Cipolla MJ. Resistance artery vasodilation to magnesium sulfate during pregnancy and the postpartum state. Am J Physiol Heart Circ Physiol. 2005;288(4):H1521–H1525.

    Article  CAS  PubMed  Google Scholar 

  15. Liao QP, Buhimschi IA, Saade G, Chwalisz K, Garfield RE. Regulation of vascular adaptation during pregnancy and post-partum: effects of nitric oxide inhibition and steroid hormones. Hum Reprod. 1996;11(12):2777–2784.

    Article  CAS  PubMed  Google Scholar 

  16. Pacher P, Ungvari Z, Nanasi PP, Mucha I, Kecskeméti V, Losonczy G. Post-partum prolongation of the atrial repolarization in rabbit. Acta Physiol Scand. 1999;166(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  17. Umar S, Nadadur R, Iorga A, Amjedi M, Matori H, Eghbali M. Cardiac structural and hemodynamic changes associated with physiological heart hypertrophy of pregnancy are reversed post-partum. J Appl Physiol (1985). 2012;113(8):1253–1259.

    Article  Google Scholar 

  18. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 2004;5(3):266–271.

    Article  CAS  PubMed  Google Scholar 

  19. Kahn DA, Baltimore D. Pregnancy induces a fetal antigen-specific maternal T regulatory cell response that contributes to tolerance. Proc Natl Acad Sci USA. 2010;107(20):9299–9304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Moldenhauer LM, Diener KR, Thring DM, Brown MP, Hayball JD, Robertson SA. Cross-presentation of male seminal fluid antigens elicits t cell activation to initiate the female immune response to pregnancy. J Immunol. 2009;182(12):8080–8093.

    Article  CAS  PubMed  Google Scholar 

  21. Norton MT, Fortner KA, Bizargity P, Bonney EA. Pregnancy alters the proliferation and apoptosis of mouse splenic ery-throid lineage cells and leukocytes. Biol Reprod. 2009;81(3):457–464.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Norton MT, Fortner KA, Oppenheimer KH, et al. Evidence that CD8 T-cell homeostasis and function remain intact during murine pregnancy. Immunology. 2010;131(3):426–437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bonney EA, Shepard MT, Bizargity P. Transient modification within a pool of CD4 T cells in the maternal spleen. Immunology. 2011;134(3):270–280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Oh MJ, Croy BA. A map of relationships between uterine natural killer cells and progesterone receptor expressing cells during mouse pregnancy. Placenta. 2008;29(4):317–323.

    Article  CAS  PubMed  Google Scholar 

  25. Constantin CM, Masopust D, Gourley T, et al. Normal establishment of virus-specific memory CD8 T cell pool following primary infection during pregnancy. J Immunol. 2007;179(7):4383–4389.

    Article  CAS  PubMed  Google Scholar 

  26. Case LK, Del Rio R, Bonney EA, et al. The postnatal maternal environment affects autoimmune disease susceptibility in A/J mice. Cell Immunol. 2010;260(2):119–127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shepard MT, Bonney EA. PD-1 regulates T cell proliferation in a tissue and subset-specific manner during normal mouse pregnancy. Immunol Invest. 2013;42(5):385–408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chen T, Darrasse-Jeze G, Bergot AS, et al. Self-specific memory regulatory T cells protect embryos at implantation in mice. J Immunol. 2013;191(5):2273–2281.

    Article  CAS  PubMed  Google Scholar 

  29. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature. 2012;490(7418):102–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Deepthi G, Chaithri PK, Latha P, et al. TGFB1 Functional Gene Polymorphisms (C-509T and T869C) in the Maternal Susceptibility to Pre-eclampsia in South Indian Women. Scand J Immunol. 2015;82(4):390–397.

    Article  CAS  PubMed  Google Scholar 

  31. van Rijn BB, Bruinse HW, Veerbeek JH, et al. Postpartum circulating markers of inflammation and the systemic acute-phase response after early-onset preeclampsia. Hypertension. 2016;67(2):404–414.

    Article  PubMed  CAS  Google Scholar 

  32. Wallace K, Cornelius DC, Scott J, et al. CD4þ T cells are important mediators of oxidative stress that cause hypertension in response to placental ischemia. Hypertension. 2014;64(5):1151–1158.

    Article  CAS  PubMed  Google Scholar 

  33. Wallace K, Novotny S, Heath J, et al. Hypertension in response to CD4(þ) T cells from reduced uterine perfusion pregnant rats is associated with activation of the endothelin-1 system. Am J Physiol Regul Integr Comp Physiol. 2012;303(2):R144–R149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wallace K, Richards S, Dhillon P, et al. CD4þ T-helper cells stimulated in response to placental ischemia mediate hypertension during pregnancy. Hypertension. 2011;57(5):949–955.

    Article  CAS  PubMed  Google Scholar 

  35. Xia Y, Kellems RE. Angiotensin receptor agonistic autoantibo-dies and hypertension: preeclampsia and beyond. Circ Res. 2013;113(1):78–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bizargity P, Del Rio R, Phillippe M, Teuscher C, Bonney EA. Resistance to lipopolysaccharide-induced preterm delivery mediated by regulatory T cell function in mice. Biol Reprod. 2009;80(5):874–881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Burke SD, Barrette VF, Carter AL, Gravel J, Adams MA, Croy BA. Cardiovascular adaptations of pregnancy in T and B cell-deficient mice. Biol Reprod. 2011;85(3):605–614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. Rag-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68(5):869–877.

    Article  CAS  PubMed  Google Scholar 

  39. Bonney EA, Onyekwuluje J. The H-Y response in mid-gestation and long after delivery in mice primed before pregnancy. Immunol Invest. 2003;32(1-2):71–81.

    Article  CAS  PubMed  Google Scholar 

  40. Bonney EA, Matzinger P. The maternal immune system’s interaction with circulating fetal cells. J Immunol. 1997;158(1):40–47.

    CAS  PubMed  Google Scholar 

  41. Lissauer D, Piper K, Goodyear O, Kilby MD, Moss PA. Fetal-specific CD8þ cytotoxic T cell responses develop during normal human pregnancy and exhibit broad functional capacity. J Immunology. 2012;189(2):1072–1080.

    Article  CAS  Google Scholar 

  42. Barrat F, Lesourd BM, Louise A, et al. Surface antigen expression in spleen cells of C57Bl/6 mice during ageing: influence of sex and parity. Clin Exp Immunol. 1997;107(3):593–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Weinzierl AO, Maurer D, Altenberend F, et al. A cryptic vascular endothelial growth factor T-cell epitope: identification and characterization by mass spectrometry and T-cell assays. Cancer Res. 2008;68(7):2447–2454.

    Article  CAS  PubMed  Google Scholar 

  44. Kolbus D, Ramos OH, Berg KE, et al. CD8+ T cell activation predominate early immune responses to hypercholesterolemia in Apoe(-)(/)(-) mice. BMC Immunol. 2010;11:58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Leonard S, Croy BA, Murrant CL. Arteriolar reactivity in lymphocyte-deficient mice. Am J Physiol Heart Circ Physiol. 2011;301(4):H1276–H1285.

    Article  CAS  PubMed  Google Scholar 

  46. Kvakan H, Kleinewietfeld M, Qadri F, et al. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation. 2009;119(22):2904–2912. doi:org/10.1161/CIRCULATIO-NAHA.108.832782.

    Article  CAS  PubMed  Google Scholar 

  47. Bu DX, Tarrio M, Maganto-Garcia E, et al. Impairment of the programmed cell death-1 pathway increases atherosclerotic lesion development and inflammation. Arterioscler Thromb Vasc Biol. 2011;31(5):1100–1107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hwang Y, Yu HT, Kim DH, et al. Expansion of CD8(+) T cells lacking the IL-6 receptor alpha chain in patients with coronary artery diseases (CAD). Atherosclerosis. 2016;249:44-51.

    Article  CAS  PubMed  Google Scholar 

  49. Libby P, Lichtman Andrew H, Hansson Göran K. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity. 2013;38(6):1092–1104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Przybyl L, Ibrahim T, Haase N, et al. Regulatory T cells ameliorate intrauterine growth retardation in a transgenic rat model for preeclampsia. Hypertension. 2015;65(6):1298–1306.

    Article  CAS  PubMed  Google Scholar 

  51. Ait-Oufella H, Salomon BL, Potteaux S, et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12(2):178–180.

    Article  CAS  PubMed  Google Scholar 

  52. Matrougui K, Abd Elmageed Z, Kassan M, et al. Natural regulatory T cells control coronary arteriolar endothelial dysfunction in hypertensive mice. Am J Pathol. 2011;178(1):434–441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Li M, Lin J, Wang Z, He S, Ma X, Li D. Oxidized low-density lipoprotein-induced proinflammatory cytokine response in macrophages are suppressed by CD4CD25(+)Foxp3(+) regulatory T cells through downregulating toll like receptor 2-mediated activation of NF-kappaB. Cell Physiol Biochem. 2010;25(6):649–656.

    Article  CAS  PubMed  Google Scholar 

  54. Nilsson J, Wigren M, Shah PK. Regulatory T cells and the control of modified lipoprotein autoimmunity-driven atherosclerosis. Trends Cardiovasc Med. 2009;19(8):272–276.

    Article  CAS  PubMed  Google Scholar 

  55. Wang Q, Strong J, Killeen N. Homeostatic competition among T cells revealed by conditional inactivation of the mouse Cd4 gene. J Exp Med. 2001;194(12):1721–1730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Christensen KL, Mulvany MJ. Mesenteric arcade arteries contribute substantially to vascular resistance in conscious rats. J Vasc Res. 1993;30(20):73–79.

    Article  CAS  PubMed  Google Scholar 

  57. Rahemtulla A, Fung-Leung WP, Schilham MW, et al. Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature. 1991;353(6340):180–184.

    Article  CAS  PubMed  Google Scholar 

  58. Phillips JK, Vance AM, Raj RS, et al. Impact of experimental diabetes on the maternal uterine vascular remodeling during rat pregnancy. Reprod Sci. 2012;19(3):322–331.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Guzik TJ, Hoch NE, Brown KA, et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204(10):2449–2460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev. 1997;159:105-117.

    Article  CAS  PubMed  Google Scholar 

  61. Shacklett BL, Cox CA, Sandberg JK, Stollman NH, Jacobson MA, Nixon DF. Trafficking of human immunodeficiency virus type 1-specific CD8+ T cells to gut-associated lymphoid tissue during chronic infection. J Virol. 2003;77(10):5621–5631.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Walch JM, Zeng Q, Li Q, et al. Cognate antigen directs CD8+ T cell migration to vascularized transplants. J Clin Invest. 2013;123(6):2663–2671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Dimayuga P, Cercek B, Oguchi S, et al. Inhibitory effect on arterial injury-induced neointimal formation by adoptive B-cell transfer in Rag-1 knockout mice. Arterioscler Thromb Vasc Biol. 2002;22(4):644–649.

    Article  CAS  PubMed  Google Scholar 

  64. Kelly BA, Bond BC, Poston L. Aortic adaptation to pregnancy: elevated expression of matrix metalloproteinases-2 and -3 in rat gestation. Mol Hum Reprod. 2004;10(5):331–337.

    Article  CAS  PubMed  Google Scholar 

  65. Walther T, Voss A, Baumert M, et al. Cardiovascular variability before and after delivery: recovery from arterial stiffness in women with preeclampsia 4 days post partum. Hypertens Pregnancy. 2014;33(1):1–14.

    Article  PubMed  Google Scholar 

  66. Dong Y, Betancourt A, Chauhan M, et al. Pregnancy Increases Relaxation in Human Omental Arteries to the CGRP Family of Peptides. Biol Reprod. 2015;134(6):134.

    Google Scholar 

  67. Bruckmann A, Seeliger C, Lehmann T, Schleußner E, Schlembach D. Altered retinal flicker response indicates microvascular dysfunction in women with preeclampsia. Hypertension. 2015;66(4):900–905.

    Article  PubMed  CAS  Google Scholar 

  68. Pruthi D, Khankin EV, Blanton RM, et al. Exposure to experimental preeclampsia in mice enhances the vascular response to future injury. Hypertension. 2015;65(4):863–870.

    Article  CAS  PubMed  Google Scholar 

  69. Garovic VD, Bailey KR, Boerwinkle E, et al. Hypertension in pregnancy as a risk factor for cardiovascular disease later in life. J Hypertension. 2010;28(4):826–833.

    Article  CAS  Google Scholar 

  70. Ngo A, Chen J, Figtree G, Morris JM, Roberts CL. Preterm birth and future risk of maternal cardiovascular disease - is the association independent of smoking during pregnancy? BMC Pregnancy Childbirth. 2015;15:1–11.

    Article  CAS  Google Scholar 

  71. Robbins CL, Hutchings Y, Dietz PM, Kuklina EV, Callaghan WM. History of preterm birth and subsequent cardiovascular disease: a systematic review. Am J Obstet Gynecol. 2014;210(4):285–297.

    Article  PubMed  Google Scholar 

  72. Bonamy AKE, Parikh NI, Cnattingius S, Ludvigsson JF, Ingelsson E. Birth characteristics and subsequent risks of maternal cardiovascular disease: effects of gestational age and fetal growth. Circulation. 2011;124(25):2839–2846.

    Article  PubMed  Google Scholar 

  73. Gunderson EP, Chiang V, Pletcher MJ, et al. History of gestational diabetes mellitus and future risk of atherosclerosis in mid-life: the coronary artery risk development in young adults study. J Am Heart Asso. 2014;3(2):e000490.

    Google Scholar 

  74. Ness RB, Harris T, Cobb J, et al. Number of pregnancies and the subsequent risk of cardiovascular disease. N Eng J Med. 1993;328(21):1528–1533.

    Article  CAS  Google Scholar 

  75. Bonney EA, Krebs K, Saade G, et al. Differential senescence in feto-maternal tissues during mouse pregnancy. Placenta. 2016; 43:26–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Conrad KP, Shroff SG. Effects of relaxin on arterial dilation, remodeling, and mechanical properties. Curr Hypertens Rep. 2011;13(6):409–420.

    Article  CAS  PubMed  Google Scholar 

  77. Liu A, Tian L, Golob M, et al. 17beta-Estradiol Attenuates Conduit Pulmonary Artery Mechanical Property Changes With Pulmonary Arterial Hypertension. Hypertension. 2015;66(5):1082–1088.

    Article  CAS  PubMed  Google Scholar 

  78. Le VP, Yamashiro Y, Yanagisawa H, Wagenseil JE. Measuring, reversing, and modeling the mechanical changes due to the absence of Fibulin-4 in mouse arteries. Biomech Model Mechanobiol. 2014;13(5):1081–1095.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Dimayuga PC, Chyu KY, Kirzner J, et al. Enhanced neointima formation following arterial injury in immune deficient Rag-1-/-mice is attenuated by adoptive transfer of CD8 T cells. PLoS One. 2011;6(5):e20214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ji H, Zheng W, Li X, et al. Sex-specific T-cell regulation of angiotensin II-dependent hypertension. Hypertension. 2014;64(3):573–582.

    Article  CAS  PubMed  Google Scholar 

  81. Schluns KS, Kieper WC, Jameson SC, Lefrançois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol. 2000;1(5):426–432.

    Article  CAS  PubMed  Google Scholar 

  82. Kitaya K, Yasuo T. Regulatory role of membrane-bound form interleukin-15 on human uterine microvascular endothelial cells in circulating CD16(-) natural killer cell extravasation into human endometrium. Biol Reprod. 2013;89(3):70.

    Article  PubMed  CAS  Google Scholar 

  83. Okada H, Nakajima T, Sanezumi M, Ikuta A, Yasuda K, Kanzaki H. Progesterone enhances interleukin-15 production in human endometrial stromal cells in vitro. J Clin Endocrinol Metab. 2000;85(12):4765–4770.

    CAS  PubMed  Google Scholar 

  84. Oelert T, Papatriantafyllou M, Pougialis G, Hämmerling GJ, Arnold B, Schüler T. Irradiation and IL-15 promote loss of CD8 T-cell tolerance in response to lymphopenia. Blood. 2010;115(11):2196–2202.

    Article  CAS  PubMed  Google Scholar 

  85. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med. 2005;202(7):907–912.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Mackay LK, Rahimpour A, Ma JZ, et al. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat Immunol. 2013;14(12):1294–1301.

    Article  CAS  PubMed  Google Scholar 

  87. Aasa KL, Zavan B, Luna RL, et al. Placental growth factor influences maternal cardiovascular adaptation to pregnancy in mice. Biol Reprod. 2015;92(2):44.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Reproductive Science Research, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Vermont, College of Medicine, Given Building Rm C-246, 89 Beaumont Avenue, Burlington, VT, 05405, USA

    Elizabeth A. Bonney MD, MPH, Ann Howard BS, Kendall Krebs BS, Kelly Begin BS, Kelsey Veilleux BS & Natalia I. Gokina PhD

Authors
  1. Elizabeth A. Bonney MD, MPH
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann Howard BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kendall Krebs BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kelly Begin BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kelsey Veilleux BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natalia I. Gokina PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth A. Bonney MD, MPH.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bonney, E.A., Howard, A., Krebs, K. et al. Impact of Immune Deficiency on Remodeling of Maternal Resistance Vasculature 4 Weeks Postpartum in Mice. Reprod. Sci. 24, 514–525 (2017). https://doi.org/10.1177/1933719116678691

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719116678691

Keywords

Search

Navigation