The Institute of Biotechnology, Academy of Sciences of the Czech Republic, Prague, Czech Republic.
Reprod Biol Endocrinol. 2012 Nov 23;10:97. doi: 10.1186/1477-7827-10-97.
The immune system plays an important role in the regulation of tissue homeostasis ("tissue immune physiology"). Function of distinct tissues during adulthood, including the ovary, requires (1) Renewal from stem cells, (2) Preservation of tissue-specific cells in a proper differentiated state, which differs among distinct tissues, and (3) Regulation of tissue quantity. Such morphostasis can be executed by the tissue control system, consisting of immune system-related components, vascular pericytes, and autonomic innervation. Morphostasis is established epigenetically, during morphogenetic (developmental) immune adaptation, i.e., during the critical developmental period. Subsequently, the tissues are maintained in a state of differentiation reached during the adaptation by a "stop effect" of resident and self renewing monocyte-derived cells. The later normal tissue is programmed to emerge (e.g., late emergence of ovarian granulosa cells), the earlier its function ceases. Alteration of certain tissue differentiation during the critical developmental period causes persistent alteration of that tissue function, including premature ovarian failure (POF) and primary amenorrhea. In fetal and adult human ovaries the ovarian surface epithelium cells called ovarian stem cells (OSC) are bipotent stem cells for the formation of ovarian germ and granulosa cells. Recently termed oogonial stem cells are, in reality, not stem but already germ cells which have the ability to divide. Immune system-related cells and molecules accompany asymmetric division of OSC resulting in the emergence of secondary germ cells, symmetric division, and migration of secondary germ cells, formation of new granulosa cells and fetal and adult primordial follicles (follicular renewal), and selection and growth of primary/preantral, and dominant follicles. The number of selected follicles during each ovarian cycle is determined by autonomic innervation. Morphostasis is altered with advancing age, due to degenerative changes of the immune system. This causes cessation of oocyte and follicular renewal at 38 +/-2 years of age due to the lack of formation of new granulosa cells. Oocytes in primordial follicles persisting after the end of the prime reproductive period accumulate genetic alterations resulting in an exponentially growing incidence of fetal trisomies and other genetic abnormalities with advanced maternal age. The secondary germ cells also develop in the OSC cultures derived from POF and aging ovaries. In vitro conditions are free of immune mechanisms, which prevent neo-oogenesis in vivo. Such germ cells are capable of differentiating in vitro into functional oocytes. This may provide fresh oocytes and genetically related children to women lacking the ability to produce their own follicular oocytes. Further study of "immune physiology" may help us to better understand ovarian physiology and pathology, including ovarian infertility caused by POF or by a lack of ovarian follicles with functional oocytes in aging ovaries. The observations indicating involvement of immunoregulation in physiological neo-oogenesis and follicular renewal from OSC during the fetal and prime reproductive periods are reviewed as well as immune system and age-independent neo-oogenesis and oocyte maturation in OSC cultures, perimenopausal alteration of homeostasis causing disorders of many tissues, and the first OSC culture clinical trial.
免疫系统在组织动态平衡的调节中起着重要作用(“组织免疫生理学”)。成年期不同组织的功能,包括卵巢,需要(1)由干细胞更新,(2)在适当分化的状态下保存组织特异性细胞,这在不同组织之间有所不同,以及(3)调节组织数量。这种形态平衡可以由包含免疫系统相关成分、血管周细胞和自主神经支配的组织控制系统来执行。形态平衡是通过形态发生(发育)免疫适应性建立的,即在关键的发育阶段。随后,组织通过驻留和自我更新的单核细胞衍生细胞的“停止效应”维持在适应过程中达到的分化状态。随后,正常组织被编程以出现(例如,卵巢颗粒细胞的晚期出现),其功能更早停止。在关键发育阶段改变某些组织分化会导致该组织功能的持续改变,包括卵巢早衰(POF)和原发性闭经。在胎儿和成年人类卵巢中,称为卵巢干细胞(OSC)的卵巢表面上皮细胞是形成卵巢生殖细胞和颗粒细胞的多能干细胞。最近被称为卵原干细胞的实际上不是干细胞,而是已经具有分裂能力的生殖细胞。免疫系统相关细胞和分子伴随着 OSC 的不对称分裂,导致次级生殖细胞的出现、对称分裂和次级生殖细胞的迁移、新颗粒细胞和胎儿及成年原始卵泡(卵泡更新)的形成,以及选择和生长初级/前腔卵泡和优势卵泡。每个卵巢周期中选择的卵泡数量由自主神经支配决定。随着年龄的增长,免疫系统的退行性变化会改变形态平衡。这导致卵子和卵泡更新在 38 +/-2 岁时停止,因为缺乏新颗粒细胞的形成。在主要生殖期结束后仍然存在于原始卵泡中的卵母细胞会积累遗传改变,导致随着母亲年龄的增长,胎儿三体和其他遗传异常的发生率呈指数级增长。次级生殖细胞也在源自 POF 和衰老卵巢的 OSC 培养物中发育。体外条件不受免疫机制的影响,这些机制可以防止体内的新卵子发生。这种生殖细胞能够在体外分化为功能性卵母细胞。这可能为缺乏产生自身卵泡卵母细胞能力的女性提供新鲜卵母细胞和遗传相关的儿童。进一步研究“免疫生理学”可能有助于我们更好地理解卵巢生理学和病理学,包括由 POF 或由衰老卵巢中具有功能性卵母细胞的卵泡缺乏引起的卵巢不孕。本文综述了参与胎儿和主要生殖期 OSC 中生理新卵子发生和卵泡更新的免疫调节的观察结果,以及 OSC 培养物中免疫和年龄独立的新卵子发生和卵母细胞成熟、围绝经期引起的许多组织失调的动态平衡改变,以及第一个 OSC 培养物临床试验。