Heme oxygenase/carbon monoxide in the female reproductive system: an overlooked signalling pathway

. 2017 ; 8 (1) : 1-12. [epub] 20170115

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid28123837

For a long time, carbon monoxide (CO) was known for its toxic effect on organisms. But there are still many things left to discover on that molecule. CO is formed directly in the body by the enzymatic activity of heme oxygenase (HO). CO plays an important role in many physiological processes, such as cell protections (against various stress factors), and the regulation of metabolic processes. Recent research proves that CO also operates in the female reproductive system. At the centre of interest is the importance of CO for gestation. During the gestation period, CO is an important element affecting the proper function of the feto-placental unit and generally affects fetal survivability rates. Gestation is one of the most important processes of successful reproduction, although there are more relevant processes that need to be researched. While already proven that CO influences steroidogenesis and the corpus luteum survivability rate, our knowledge concerning the function and importance of CO in the reproductive system is still relatively limited. As an example, our knowledge of CO function in an oocyte, the most important cell for reproduction, is almost non-existent. The aim of this review is to summarize our current knowledge concerning the function of CO in the female reproductive system.

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Palmer RJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524–526. PubMed

Ignarro LJ, Byrns RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res. 1987;61:866–879. PubMed

Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci U S A. 1968;61:748–755. PubMed PMC

Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem. 1969;244:6388–6394. PubMed

Stewart RD. The effect of carbon monoxide on humans. Annu Rev Pharmacol. 1975;15:409–423. PubMed

Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger. Science. 1993;259:381–384. PubMed

Rattan S, Chakder S. Inhibitory effect of CO on internal anal sphincter: Heme oxygenase inhibitor inhibits NANC relaxation. Am J Physiol. 1993;265:799–804. PubMed

Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev. 2005;57:585–630. PubMed

Rotenberg MO, Maines MD. Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes: possible heme-binding site? Arch Biochem Biophys. 1991;290:336–344. PubMed

Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517–554. PubMed

McCoubrey WK, Maines MD. Domains of rat heme oxygenase-2: the amino terminus and histidine 151 are required for heme oxidation. Arch Biochem Biophys. 1993;302:402–408. PubMed

Shibahara S, Muller R, Taguchi H, Yoshida T. Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci U S A. 1985;82:7865–7869. PubMed PMC

Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem. 1986;261:411–419. PubMed

Yoshida T, Kikuchi G. Purification and properties of heme oxygenase from pig spleen microsomes. J Biol Chem. 1978;253:4224–4229. PubMed

Dunn LL, Midwinter RG, Ni J, Hamid HA, Parish CR, Stocker R. New insights into intracellular locations and functions of heme oxygenase-1. Antioxid Redox Signal. 2014;20:1723–1742. PubMed PMC

Biswas C, Shah N, Muthu M, La P, Fernando AP, Sengupta S, Zang G, Dennery PA. Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses. J Biol Chem. 2014;289:26882–26894. PubMed PMC

Ryter SW, Choi AK. Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Transl Res. 2016;167:7–34. PubMed PMC

Kim YM, Pae HO, Park JE, Lee YC, Woo JM, Kim NH, Choi YK, Lee BS, Kim SR, Chung HT. Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal. 2011;14:137–167. PubMed PMC

Hori R, Kashiba M, Toma T, Yachie A, Goda N, Makino N, Soejima A, Nagasawa T, Nakabayashi K, Suematsu M. Gene transfection of H25A mutant heme oxygenase-1 protects cells against hydroperoxide-induced cytotoxicity. J Biol Chem. 2002;277:10712–10718. PubMed

Dennery PA. Signaling function of heme oxygenase proteins. Antioxid Redox Signal. 2014;20:1743–1753. PubMed PMC

Ma N, Ding X, Doi M, Izumi N, Semba R. Cellular and subcellular localization of heme oxygenase-2 in monkey retina. J Neurocytol. 2004;33:407–415. PubMed

West AR, Oates PS. Subcellular location of heme oxygenase 1 and 2 and divalent metal transporter 1 in relation to endocytotic markers during heme iron absorption. J Gastroen Hepatol. 2007;23:150–158. PubMed

Liu N, Wang X, McCoubrey WK, Maines MD. Developmentally regulated expression of two transcripts for heme oxygenase-2 with a first exon unique to rat testis: control by corticosterone of the oxygenase protein expression. Gene. 2000;241:175–183. PubMed

Turkseven S, Drummond G, Rezzani R, Rodella L, Quan S, Ikehara S, Abraham NG. Impact of silencing HO-2 on EC-SOD and the mitochondrial signaling pathway. J Cell Biochem. 2007;100:815–823. PubMed

Muñoz-Sánchez J, Chánez-Cárdenas ME. A review on hemeoxygenase-2: focus on cellular protection and oxygen response. Oxid Med Cell Longev. 2014;2014:604981. PubMed PMC

Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M. Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene. 2004;336:241–250. PubMed

Boczkowski J, Poderoso JJ, Motterlini R. CO-metal interaction: vital signaling from a lethal gas. Trends Biochem Sci. 2006;31:614–621. PubMed

Tsiftsoglou AS, Tsamadou AI, Papadopoulou LC. Heme as key regulator of major mammalian cellular functions: molecular, cellular, and pharmacological aspects. Pharmacol Ther. 2006;111:327–345. PubMed

Roberts GP, Youn H, Kerby RL. CO-sensing mechanisms. Microbiol Mol Biol Rev. 2004;68:453–473. PubMed PMC

Furchgott RF, Jothianandan D. Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels. 1991;28:52–61. PubMed

Stone JR, Marletta MA. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry. 1994;33:5636–5640. PubMed

Ishimaru R, Leung K, Hong L, LaPolt PS. Inhibitory effects of nitric oxide on estrogen production and cAMP levels in rat granulosa cell cultures. J Endocrinol. 2001;168:249–255. PubMed

Grasselli F, Ponderato N, Basini G, Tamanini C. Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulosa cells. Domest Anim Endocrin. 2001;20:241–252. PubMed

Schwarz KR, Pires PR, Mesquita LG, Chiaratti MR, Leal CL. Effect of nitric oxide on the cyclic guanosine monophosphate (cGMP) pathway during meiosis resumption in bovine oocytes. Theriogenology. 2014;81:556–564. PubMed

Alexandreanu IC, Lawson DM. Heme oxygenase in the rat ovary: immunohistochemical localization and possible role in steroidogenesis. Exp Biol Med (Maywood) 2003;228:59–63. PubMed

Ingi T, Cheng J, Ronnett GV. Carbon monoxide: an endogenous modulator of the nitric oxide-cyclic GMP signaling system. Neuron. 1996;16:835–842. PubMed

Kim HS, Loughran PA, Billiar TR. Carbon monoxide decreases the level of iNOS protein and active dimer in IL-1β-stimulated hepatocytes. Nitric Oxide. 2008;18:256–265. PubMed PMC

Motterlini R, Green CJ, Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal. 2002;4:615–624. PubMed

Bu S, Xia G, Tao Y, Lei L, Zhou B. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol Cell Endocrinol. 2003;207:21–30. PubMed

Tichovská H, Petr J, Chmelíková E, Sedmíková M, Tůmová L, Krejčová M, Dorflerova A, Rajmon R. Nitric oxide and meiotic competence of porcine oocytes. Animal. 2011;5:1398–1405. PubMed

Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med. 2008;86:267–279. PubMed

D’Amico G, Lam F, Hagen T, Moncada S. Inhibition of cellular respiration by endogenously produced carbon monoxide. J Cell Sci. 2006;119:2291–2298. PubMed

Taillé C, El-Benna J, Lanone S, Boczkowski J, Motterlini R. Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J Biol Chem. 2005;280:25350–25360. PubMed

Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res. 2008;103:1232–1240. PubMed PMC

Suliman HB, Carraway MS, Tatro LG, Piantadosi CA. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci. 2007;120:299–308. PubMed

Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barrière P, Malthièry Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–429. PubMed

Finkel T. Oxygen radicals and signaling. Curr Opin Cell Biol. 1998;10:248–253. PubMed

Combelles CH, Gupta S, Agarwal A. Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online. 2009;18:864–880. PubMed PMC

Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86:583–650. PubMed

Kim HP, Ryter SW, Choi AK. Co as a cellular signaling molecule. Annu Rev Pharmacol. 2006;46:411–449. PubMed

Bilban M, Bach FH, Otterbein SL, Ifedigbo E, Costa d’Avila J, Esterbauer H, Chin BY, Usheva A, Robson SC, Wagner O, Otterbein LE. Carbon monoxide orchestrates a protective response through PPARγ. Immunity. 2006;24:601–610. PubMed

Wang R, Wang Z, Wu L, Hanna ST, Peterson-Wakeman R. Reduced vasorelaxant effect of carbon monoxide in diabetes and the underlying mechanisms. Diabetes. 2001;50:166–174. PubMed

Ou XH, Li S, Xu BZ, Wang ZB, Quan S, Li M, Zhang QH, Ouyang YC, Schatten H, Xing FQ, Sun QY. P38α MAPK is a MTOC-associated protein regulating spindle assembly, spindle length and accurate chromosome segregation during mouse oocyte meiotic maturation. Cell Cycle. 2014;9:4130–4143. PubMed PMC

Miyagaki Y, Kanemori Y, Tanaka F, Baba T. Possible role of p38 MAPK-MNK1-EMI2 cascade in metaphase-II arrest of mouse oocytes. Biol Reprod. 2014;91:45–53. PubMed

Nogueira D, Cortvrindt R, De Matos DG, Vanhoutte L, Smitz J. Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol Reprod. 2003;69:2045–2052. PubMed

Vanhoutte L, Nogueira D, Gerris J, Dhont M, De Sutter P. Effect of temporary nuclear arrest by Phosphodiesterase 3-Inhibitor on morphological and functional aspects of in vitro matured mouse oocytes. Mol Reprod Dev. 2008;75:1021–1030. PubMed

Wilkinson WJ, Kemp PJ. Carbon monoxide: an emerging regulator of ion channels. J Physiol. 2011;589:3055–3062. PubMed PMC

Peers C, Boyle JP, Scragg JL, Dallas ML, Al-Owais MM, Hettiarachichi NT, Elies J, Johnson E, Gamper N, Steele DS. Diverse mechanisms underlying the regulation of ion channels by carbon monoxide. Brit J Pharmacol. 2015;172:1546–1556. PubMed PMC

Lorca RA, Prabagaran M, England SK. Functional insights into modulation of BKCa channel activity to alter myometrial contractility. Front Physiol. 2014;5:289. PubMed PMC

Odrcich MJ, Graham CH, Kimura KA, McLaughlin BE, Marks GS, Nakatsu K, Brien JF. Heme oxygenase and nitric oxide synthase in the placenta of the guinea-pig during gestation. Placenta. 1998;19:509–516. PubMed

Ihara N, Akagi R, Ejiri K, Kudo T, Furuyama K, Fujita H. Developmental changes of gene expression in heme metabolic enzymes in rat placenta. FEBS Lett. 1998;439:163–167. PubMed

Kreiser D, Kelly DK, Seidman DS, Stevenson DK, Baum M, Dennery PA. Gestational pattern of heme oxygenase expression in the rat. Pediatr Res. 2003;54:172–178. PubMed

Murphy BJ, Laderoute KR, Short SM, Sutherland RM. The identification of heme oxygenase as a major hypoxic stress protein in Chinese hamster ovary cells. Brit J Cancer. 1991;64:69–73. PubMed PMC

Harada T, Koi H, Kubota T, Aso T. Haem oxygenase augments porcine granulosa cell apoptosis in vitro. J Endocrinol. 2004;181:191–205. PubMed

Pfeiffer MJ, Taher L, Drexler H, Suzuki Y, Makałowski W, Schwarzer C, Wang B, Fuellen B, Boiani M. Differences in embryo quality are associated with differences in oocyte composition: a proteomic study in inbred mice. Proteomics. 2015;15:675–687. PubMed

Maines MD, Kutty RK. Differential response of testicular and ovarian heme oxygenase activity to metal ions. Arch Biochem Biophys. 1983;226:134–144. PubMed

Cella M, Farina MG, Keller Sarmiento MI, Chianelli M, Rosenstein RE, Franchi AM. Heme oxygenase-carbon monoxide (HO-CO) system in rat uterus: effect of sexual steroids and prostaglandins. J Steroid Biochem Mol Biol. 2006;99:59–66. PubMed

Zenclussen ML, Casalis PA, Jensen F, Woidacki K, Zenclussen AC. Hormonal fluctuations during the estrous cycle modulate heme oxygenase-1 expression in the uterus. Front Endocrinol (Lausanne) 2014;5:32. PubMed PMC

Acevedo CH, Ahmed A. Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy. J Clin Invest. 1998;101:949–955. PubMed PMC

Alexandreanu IC, Lawson DM. Effects of chronic administration of a heme oxygenase substrate or inhibitor on progression of the estrous cycle, pregnancy and lactation of Sprague-Dawley rats. Life Sci. 2002;72:153–162. PubMed

Vinatier D, Dufour P, Tordjeman-Rizzi N, Prolongeau JF, Depret-Moser S, Monnier JC. Immunological aspects of ovarian function: role of the cytokines. Eur J Obstet Gynecol Reprod Biol. 1995;63:155–168. PubMed

Li L, Tang J, Sun Y, Wu J, Yu P, Wang G. Upregulation of HO-1 attenuates LPS-stimulated proinflammatory responses through downregulation of p38 signaling pathways in rat ovary. Inflammation. 2015;38:1085–1092. PubMed

Richards JS, Russell DL, Ochsner S, Espey LL. Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol. 2002;64:69–92. PubMed

Zenclussen ML, Jensen F, Rebelo S, El-Mousleh T, Casalis PA, Zenclussen AC. Heme oxzgenase-1 expression in the ovary dictates a proper oocyte ovulation, fertilization, and corpora lutea maintenance. Am J Reprod Immunol. 2012;67:376–382. PubMed

Devoto L, Vega M, Kohen P, Castro O, Carvallo P, Palomino A. Molecular regulation of progesterone secretion by the human corpus luteum throughout the menstrual cycle. J Reprod Immunol. 2002;55:11–20. PubMed

Vreman HJ, Zentner AR, Wong RJ, Stevenson DK. Carbon monoxide production and upregulation of heme oxygenase activity in mice after heme administration. Pediatr Res. 1999;4:231A–231A.

Chen B, Guo L, Fan C, Bolisetty S, Joseph R, Wright MM, Agarwal A, George JF. Carbon monoxide rescues heme oxygenase-1-deficient mice from arterial thrombosis in allogeneic aortic transplantation. Am J Pathol. 2009;175:422–429. PubMed PMC

Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AK, Soares MP. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 2000;192:1015–1026. PubMed PMC

Bergandi L, Basso G, Evangelista F, Canosa S, Dalmasso P, Aldieri E, Revelli A, Benedetto C, Ghigo D. Inducible nitric oxide synthase and heme oxygenase 1 are expressed in human cumulus cells and may be used as biomarkers of oocyte competence. Reprod Sci. 2014;21:1370–1377. PubMed

Zenclussen ML, Casalis PA, El-Mousleh T, Rebelo S, Langwisch S, Linzke N, Volk HD, Fest S, Soares MP, Zenclussen AC. Haem oxygenase-1 dictates intrauterine fetal survival in mice via carbon monoxide. J Pathol. 2011;225:293–304. PubMed

Bainbridge SA, Smith GN. HO in pregnancy. Free Radical Bio Med. 2005;38:979–988. PubMed

Levytska K, Kingdom J, Baczyk D, Drewlo S. Heme oxygenase-1 in placental development and pathology. Placenta. 2013;34:291–298. PubMed

George EM, Granger JP. Heme oxygenase in pregnancy and preeclampsia. Curr Opin Nephrol Hypertens. 2013;22:156–162. PubMed PMC

Zenclussen ML, Linzke N, Schumacher A, Fest S, Meyer N, Casalis PA, Zenclussen AC. Heme oxygenase-1 is critically involved in placentation, spiral artery remodeling, and blood pressure regulation during murine pregnancy. Front Pharmacol. 2015;5:291. PubMed PMC

Schumacher A, Zenclussen AC. Effects of heme oxygenase-1 on innate and adaptive immune responses promoting pregnancy success and allograft tolerance. Front Pharmacol. 2015;5:288. PubMed PMC

Yoshiki N, Kubota T, Aso T. Expression and localization of heme oxygenase in human placental villi. Biochem Bioph Res Co. 2000;276:1136–1142. PubMed

Zenclussen AC, Joachim R, Hagen E, Peiser C, Klapp BF, Arck PC. Heme oxygenase is downregulated in stress-triggered and interleukin-12-mediated murine abortion. Scand J Immunol. 2002;55:560–569. PubMed

Zenclussen AC, Sollwedel A, Zambon Bertoja AZ, Gerlof K, Zenclussen ML, Woiciechowsky C, Volk HD. Heme oxygenase as a therapeutic target in immunological pregnancy complications. Int Immunopharmacol. 2005;5:41–51. PubMed

Zenclussen AC, Lim E, Knoeller S, Knackstedt M, Hertwig K, Hagen E, Klapp BF, Arck PC. Heme oxygenases in pregnancy II: HO-2 is downregulated in human pathologic pregnancies. Am J Reprod Immunol. 2003;50:66–76. PubMed

Lash GE, McLaughlin BE, MacDonald-Goodfellow SK, Smith GN, Brien JF, Marks GS, Nakatsu K, Graham CH. Relationship between tissue damage and heme oxygenase expression in chorionic villi of term human placenta. Am J Physiol Heart C Physiol. 2003;284:H160–H167. PubMed

Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A. 1994;98:10919–10924. PubMed PMC

Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK. Effect of heme oxygenase-1 deficiency on placental development. Placenta. 2009;30:861–868. PubMed PMC

Song H, Lim H, Paria BC, Matsumoto H, Swift LL, Morrow J, Bonventre JV, Dey SK. Cytosolic phospholipase A 2 α is crucial for ‘on-time’ embryo implantation that directs subsequent development. Development. 2002;129:2789–2889. PubMed

Linzke N, Schumacher A, Woidacki K, Croy BA, Zenclussen AC. Carbon monoxide promotes proliferation of uterine natural killer cells and remodeling of spiral arteries in pregnant hypertensive heme oxygenase-1 mutant mice. Hypertension. 2014;63:580–588. PubMed

Solano ME, Kowal MK, O’Rourke GE, Horst AK, Modest K, Plösch T, Barikbin R, Remus CC, Berger RG, Jago C, Ho H, Sass G, Parker VJ, Lzdon JP, DeMayo FJ, Hecher K, Karimi K, Arck PC. Progesterone and HMOX-1 promote fetal growth by CD8 T cell modulation. J Clin Invest. 2015;125:1726–1738. PubMed PMC

Hatta K, Carter AL, Chen Z, Leno-Duran E, Ruiz-Ruiz C, Olivares EG, Tse MY, Pagn SC, Croy BA. Expression of the vasoactive proteins AT1, AT2, and ANP by pregnancy-induced mouse uterine natural killer cells. Reprod Sci. 2011;18:383–390. PubMed

Zhao H, Azuma J, Kalish F, Wong RJ, Stevenson DK. Maternal heme oxygenase 1 regulates placental vasculature development via angiogenic factors in mice. Biol Reprod. 2011;85:1005–1012. PubMed PMC

Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devery LR, Wigmore SJ, Abbas A, Hewett PW, Ahmed A. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation. 2007;115:1789–1797. PubMed

Sollwedel A, Bertoja AZ, Zenclussen ML, Gerlof K, Lisewski U, Wafula P, Sawityki B, Woiciechowsky C, Volk HD, Zenclussen AC. Protection from abortion by heme oxygenase-1 up-regulation is associated with increased levels of Bag-1 and Neuropilin-1 at the fetal-maternal interface. J Immunol. 2005;175:4875–4885. PubMed

Schumacher A, Wafula PO, Teles A, El-Mousleh T, Linzke N, Zenclussen ML, Langwisch S, Heinze K, Wollenberg I, Casalis PA, Volk HD, Fest S, Zenclussen AC. Blockage of heme oxygenase-1 abrogates the protective effect of regulatory T cells on murine pregnancy and promotes the maturation of dendritic cells. PLoS One. 2012;7:e42301. PubMed PMC

Zenclussen AC, Schumacher A, Zenclussen ML, Wafula P, Volk HD. Immunology of pregnancy: cellular mechanisms allowing fetal survival within the maternal uterus. Exprt Rev Mol Med. 2007;9:1–14. PubMed

Zenclussen ML, Anegon I, Bertoja AZ, Chauveau C, Vogt K, Gerlof K, Sollwedel A, Volk HD, Ritter T, Zenclussen AC. Over-expression of heme oxygenase-1 by adenoviral gene transfer improves pregnancy outcome in a murine model of abortion. J Reprod Immunol. 2006;69:35–52. PubMed

Kreiser D, Nguyen X, Wong R, Seidman D, Stevenson D, Quan S, Abraham N, Dennery PA. Heme oxygenase-1 modulates fetal growth in the rat. Lab Invest. 2002;82:687–692. PubMed

Tachibana M, Hashino M, Nishida T, Shimizu T, Watarai M, Bereswill S. Protective role of heme oxygenase-1 in Listeria monocytogenes-induced abortion. PLoS One. 2011;6:e25046. PubMed PMC

Tachibana M, Watanabe K, Yamasaki Y, Suzuki H, Watarai M. Expression of heme oxygenase-1 is associated with abortion caused by Brucella abortus infection in pregnant mice. Microb Pathogenesis. 2008;45:105–109. PubMed

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The effect of carbon monoxide on meiotic maturation of porcine oocytes

. 2021 ; 9 () : e10636. [epub] 20210323

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