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Journal of Zhejiang University-SCIENCE B

, Volume 20, Issue 7, pp 576–587 | Cite as

Improvement in post-partum uterine involution in rats treated with Apios americana

  • Zi-huan Zheng
  • Ying Han
  • Shi-ying You
  • Zuo Chen
  • Xiao-dong ZhengEmail author
Article
  • 4 Downloads

Abstract

Objective: Apios americana, a plant used as a staple ingredient of native American diets, has various properties, including anti-cancer, anti-hyperglycemic, hypotensive, and anti-inflammatory activity. In Japan, Apios is used as a post-natal medication. After parturition, women undergo a period of recovery as they return to pre-pregnancy conditions. However, few health products that aid post-partum recovery are on the market. We explored whether Apios can accelerate the post-partum recovery process, in particular the involution of the uterus. Methods: Female rats kept in individual cages were mated with two male rats, with the exception of the control group (female rats without mating, on basal diet; n=6). After delivery, rats were divided into five groups based on their diet: basal diet (model; n=6); basal diet+oral intake at 5.4 g/kg of Chanfukang granules (a Chinese patent medicine preparation for post-partum lochia) (positive; n=6); basal diet containing 10% Apios powder (low; n=6); basal diet containing 20% Apios powder (medium; n=6); basal diet containing 40% Apios powder (high; n=6). Five days later, uteri and spleens were weighed. Uterus and spleen indices for each rat were calculated by dividing visceral weight by the total weight. Hormone and cytokine concentrations were measured using enzyme-linked immunosorbent assay (ELISA). Histological analysis of uteri was completed using hematoxylin and eosin (H&E) staining. Expression of matrix metalloproteinases and inhibitors in uteri was measured by western blotting. Results: Our results showed that Apios treatment reduced the post-partum uterus index and regulated the hormone concentrations. Moreover, we found that the process of uterine involution was accelerated, based on morphological changes in the uterus. In addition, our results indicated that Apios alleviated the inflammatory response induced by the involution process. Transforming growth factor ß was also found to be regulated by Apios. There were significant downregulation of matrix metalloproteinases and upregulation of their inhibitors by Apios, which suggested that Apios increased the rate of the collagen clearance process. Conclusions: These results, based on experimental observations at the molecular and protein levels, verified our hypothesis that Apios can improve uterine involution, and demonstrated the potential application of Apios in post-partum care.

Key words

Apios americana Uterine involution Cytokine Matrix metalloproteinase 

美国豆芋加快产后大鼠的子宫修复

中文概要

目的: 研究美国豆芋(Apios americana)对产后恢复过程,特别是子宫复旧的影响。

创新点: 开发针对产后恢复的新食品。

方法: 将雌雄大鼠配种交配,对照组除外(没有交配的雌性大鼠,基础日粮,n=6)。分娩后,将雌性大鼠分为五组:基础饮食(模型组,n=6);基础饮食+灌胃给药5.4 g/kg 的产妇康颗粒(阳性组,n=6);含10%豆芋粉末的基础日粮(低剂量组,n=6);含20%豆芋粉末的基础日粮(中剂量组,n=6);含40%豆芋粉末的基础日粮(高剂量组,n=6)。实验结束后,称量子宫和脾脏质量,计算子宫和脾脏指数。并测量血清内激素和细胞因子水平,研究子宫的组织病理学变化,检测基质金属蛋白酶和抑制剂在子宫中的表达。

结论: 豆芋干预减少了产后子宫指数并调节了激素浓度,加速了子宫形态复旧的过程,减轻了分娩引起的炎症反应。同时发现,转化生长因子β 也受豆芋调节。豆芋干预使得基质金属蛋白酶显著下调,其抑制剂则显著上调,这表明豆芋增加了胶原清除过程的速度。

关键词

美国豆芋 子宫复旧 细胞因子 基质金属蛋白酶 

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References

  1. Alan E, Liman N, 2012. Immunohistochemical localization of beta defensins in the endometrium of rat uterus during the postpartum involution period. Vet Res Commun, 36(3): 173–185.  https://doi.org/10.1007/s11259-012-9529-7 Google Scholar
  2. Al-Bassam MA, Thomson RG, O'Donnell L, 1981. Normal postpartum involution of the uterus in the dog. Can J Comp Med, 45(3):217–232.Google Scholar
  3. Alkema L, Chou D, Hogan D, et al., 2016. Global, regional, and national levels and trends in maternal mortality between 1990 and 2015, with scenario-based projections to 2030: a systematic analysis by the UN maternal mortality estimation inter-agency group. Lancet, 387(10017):462–474.  https://doi.org/10.1016/S0140-6736(15)00838-7 Google Scholar
  4. Azawi OI, 2008. Postpartum uterine infection in cattle. Anim Reprod Sci, 105(3-4):187–208.  https://doi.org/10.1016/j.anireprosci.2008.01.010 Google Scholar
  5. Chitisankul WT, Shimada K, Omizu Y, et al., 2015. Mechanism of DDMP-saponin degradation and maltol production in soymilk preparation. LWT-Food Sci Technol, 64(1): 197–204.  https://doi.org/10.1016/j.lwt.2015.05.023 Google Scholar
  6. Cui J, Kim Y, Lee EB, et al., 2016. Immunostimulatory activity of Apios tuber extract on RAW264.7 macrophage cells. J Bacteriol Virol, 46(4):248–257.  https://doi.org/10.4167/jbv.2016.46.4.248 Google Scholar
  7. Curry TE Jr, Osteen KG, 2003. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev, 24(4): 428–465.  https://doi.org/10.1210/er.2002-0005 Google Scholar
  8. Elliott L, McMahon KJ, Gier HT, et al., 1968. Uterus of the cow after parturition: bacterial content. Am J Vet Res, 29(1):77–81.Google Scholar
  9. Ferenczy A, Bertrand G, Gelfand MM, 1979. Studies on the cytodynamics of human endometrial regeneration: III. In vitro short-term incubation historadioautography. Am J Obstet Gynecol, 134(3):297–304.  https://doi.org/10.1016/S0002-9378(16)33036-8 Google Scholar
  10. Gaide Chevronnay HP, Selvais C, Emonard H, et al., 2012. Regulation of matrix metalloproteinases activity studied in human endometrium as a paradigm of cyclic tissue breakdown and regeneration. Biochim Biophys Acta (BBA) Proteins Proteom, 1824(1):146–156.  https://doi.org/10.1016/j.bbapap.2011.09.003 Google Scholar
  11. Galvão KN, Santos NR, Galvão JS, et al., 2011. Association between endometritis and endometrial cytokine expression in postpartum Holstein cows. Theriogenology, 76(2): 290–299.  https://doi.org/10.1016/j.theriogenology.2011.02.006 Google Scholar
  12. Gray CA, Bartol FF, Tarleton BJ, et al., 2001. Developmental biology of uterine glands. Biol Reprod, 65(5):1311–1323.  https://doi.org/10.1095/biolreprod65.5.1311 Google Scholar
  13. Griffin JF, Hartigan PJ, Nunn WR, 1974. Non-specific uterine infection and bovine fertility: I. Infection patterns and endometritis during the first seven weeks post-partum. Theriogenology, 1(3):91–106.  https://doi.org/10.1016/0093-691X(74)90052-1 Google Scholar
  14. Grota LJ, Eik-Nes KB, 1967. Plasma progesterone concentrations during pregnancy and lactation in the rat. J Reprod Fertil, 13(1):83–91.  https://doi.org/10.1530/jrf.0.0130083 Google Scholar
  15. Harianja WY, Setiani O, Umaroh U, et al., 2017. The impact of pineapple (Ananas comosus (L.) Merr.) juice on fundal height in primigravida mothers during postpartum period. Belitung Nurs J, 3(2):134–141.  https://doi.org/10.33546/bnj.76 Google Scholar
  16. Henell F, Ericsson JLE, Glaumann H, 1983. An electron microscopic study of the post-partum involution of the rat uterus. With a note on apparent crinophagy of collagen. Virchows Arch B Cell Pathol Incl Mol Pathol, 42(1): 271–287.  https://doi.org/10.1007/BF02890390 Google Scholar
  17. Hoshikawa K, Juliarni 1, 1995. The growth of apios (Apios americana Medikus), a new crop, under field conditions. Jpn J Crop Sci, 64(2):323–327.  https://doi.org/10.1626/jcs.64.323 Google Scholar
  18. Hulboy DL, Rudolph LA, Matrisian LM, 1997. Matrix metalloproteinases as mediators of reproductive function. Mol Hum Reprod, 3(1):27–45.  https://doi.org/10.1093/molehr/3.1.27 Google Scholar
  19. Kasimanickam RK, Kasimanickam VR, Olsen JR, et al., 2013. Associations among serum pro- and anti-inflammatory cytokines, metabolic mediators, body condition, and uterine disease in postpartum dairy cows. Reprod Biol Endocrinol, 11:103.  https://doi.org/10.1186/1477-7827-11-103 Google Scholar
  20. Kawamura J, Miura E, Kawakishi K, et al., 2015. Investigation of the safety and antihyperglycemic effect of Apios americana flower intake as a food material in normal and diabetic mice. Food Sci Technol Res, 21(3):453–462.  https://doi.org/10.3136/fstr.21.453 Google Scholar
  21. Kikuta C, Sugimoto Y, Konishi Y, et al., 2012. Physicochemical and structural properties of starch isolated from Apios americana Medikus. J Appl Glycosci, 59(1):21–30.  https://doi.org/10.5458/jag.jag.JAG-2011_011 Google Scholar
  22. Kinugasa H, Watanbe Y, 1992. Nutritional composition of the tubers of American groundnut (Apios americana Medikus). Sonoda Women’s Coll Stud, 26:209–218.Google Scholar
  23. Krishnan HB, 1998. Identification of genistein, an anticarcinogenic compound, in the edible tubers of the American groundnut (Apios americana Medikus). Crop Sci, 38(4): 1052–1056.  https://doi.org/10.2135/cropsci1998.0011183X003800040028x Google Scholar
  24. Kuramoto S, Kaneyoshi G, Morinaga Y, et al., 2013. Angiotensin-converting enzyme-inhibitory peptides isolated from pepsin hydrolyzate of Apios americana tuber and their hypotensive effects in spontaneously hypertensive rats. Food Sci Technol Res, 19(3):399–407.  https://doi.org/10.3136/fstr.19.399 Google Scholar
  25. LeBlanc MM, Hansen PJ, Buhi WC, 1988. Uterine protein secretion in postpartum and cyclic mares. Theriogenology, 29(6):1303–1316.  https://doi.org/10.1016/0093-691X(88)90010-6 Google Scholar
  26. Lin RY, Sullivan KM, Argenta PA, et al., 1995. Exogenous transforming growth factor-beta amplifies its own expression and induces scar formation in a model of human fetal skin repair. Ann Surg, 222(2):146–154.  https://doi.org/10.1097/00000658-199508000-00006 Google Scholar
  27. Manase K, Endo T, Chida M, et al., 2006. Coordinated elevation of membrane type 1-matrix metalloproteinase and matrix metalloproteinase-2 expression in rat uterus during postpartum involution. Reprod Biol Endocrinol, 4:32.  https://doi.org/10.1186/1477-7827-4-32 Google Scholar
  28. Morales MR, Foster JG, 2009. Forage potential of American potato bean. Proceedings of the American Forage and Grassland Council. 2009 Annual Conference, Grand Rapids, Michigan.Google Scholar
  29. Murphy G, Nagase H, 2008. Progress in matrix metalloproteinase research. Mol Aspects Med, 29(5):290–308.  https://doi.org/10.1016/j.mam.2008.05.002 Google Scholar
  30. Nagase H, Visse R, Murphy G, 2006. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res, 69(3):562–573.  https://doi.org/10.1016/j.cardiores.2005.12.002 Google Scholar
  31. Nara K, Nihei KI, Ogasawara Y, et al., 2011. Novel isoflavone diglycoside in groundnut (Apios americana Medik). Food Chem, 124(3):703–710.  https://doi.org/10.1016/j.foodchem.2010.05.107 Google Scholar
  32. Nguyen TTT, Shynlova O, Lye SJ, 2016. Matrix metalloproteinase expression in the rat myometrium during pregnancy, term labor, and postpartum. Biol Reprod, 95(1):24.  https://doi.org/10.1095/biolreprod.115.138248 Google Scholar
  33. O'kane S, Ferguson MWJ, 1997. Transforming growth factor ßs and wound healing. Int J Biochem Cell Biol, 29(1):63–78.  https://doi.org/10.1016/S1357-2725(96)00120-3 Google Scholar
  34. Petrovitch I, Jeffrey RB, Heerema-McKenney A, 2009. Sub-involution of the placental site. J Ultrasound Med, 28(8): 1115–1119.  https://doi.org/10.7863/jum.2009.28.8.1115 Google Scholar
  35. Reynolds B, Blackmon W, Wickremesinhe E, et al., 1988. Domestication of Apios americana. In: Janick J (Ed.), Advances in New Crops: Proceedings of the First National Symposium New Crops: Research, Development, Economics, Timber Press, p.436–442.Google Scholar
  36. Rosen T, 2008. Placenta accreta and cesarean scar pregnancy: overlooked costs of the rising cesarean section rate. Clin Perinatol, 35(3):519–529.  https://doi.org/10.1016/j.clp.2008.07.003 Google Scholar
  37. Salamonsen LA, 2003. Tissue injury and repair in the female human reproductive tract. Reproduction, 125(3):301–311.  https://doi.org/10.1530/rep.0.1250301 Google Scholar
  38. Sellers A, Woessner JF Jr, 1980. The extraction of a neutral metalloproteinase from the involuting rat uterus, and its action on cartilage proteoglycan. Biochem J, 189(3):521–531.  https://doi.org/10.1042/bj1890521 Google Scholar
  39. Sheldon IM, 2004. The postpartum uterus. Vet Clin North Am Food Anim Pract, 20(3):569–591.  https://doi.org/10.1016/j.cvfa.2004.06.008 Google Scholar
  40. Sheldon IM, Noakes DE, Rycroft AN, et al., 2002. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction, 123(6):837–845.  https://doi.org/10.1530/rep.0.1230837 Google Scholar
  41. Shimizu K, Furuya T, Takeo Y, et al., 1983. Clearance of materials from breakdown of uterine collagen in mice during postpartum involution. Acta Anat (Basel), 116(1): 10–13.  https://doi.org/10.1159/000145720 Google Scholar
  42. Shkurupiy VA, Obedinskaya KS, Nadeev AP, 2011. Morphological study of the main mechanisms of myometrium involution after repeated pregnancies in mice. Bull Exp Biol Med, 150(3):378–382.  https://doi.org/10.1007/s10517-011-1147-9 Google Scholar
  43. Soo C, Beanes SR, Hu FY, et al., 2003. Ontogenetic transition in fetal wound transforming growth factor-ß regulation correlates with collagen organization. Am J Pathol, 163(6): 2459–2476.  https://doi.org/10.1016/S0002-9440(10)63601-2 Google Scholar
  44. Takamoto N, Leppert PC, Yu SY, 1998. Cell death and proliferation and its relation to collagen degradation in uterine involution of rat. Connec Tissue Res, 37(3-4): 163–175.  https://doi.org/10.3109/03008209809002436 Google Scholar
  45. Takashima M, Nara K, Niki E, et al., 2013. Evaluation of biological activities of a groundnut (Apios americana Medik) extract containing a novel isoflavone. Food Chem, 138(1):298–305.  https://doi.org/10.1016/j.foodchem.2012.10.100 Google Scholar
  46. Umenishi F, Umeda M, Miyazaki K, 1991. Efficient purification of TIMP-2 from culture medium conditioned by human hepatoma cell line, and its inhibitory effects on metalloproteinases and in vitro tumor invasion. J Biochem, 110(2):189–195.  https://doi.org/10.1093/oxfordjournals.jbchem.a123555 Google Scholar
  47. Wang QH, Zhang S, Qin LM, et al., 2017. Yimu San improves obstetric ability of pregnant mice by increasing serum oxytocin levels and connexin 43 expression in uterine smooth muscle. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 18(11):986–993.  https://doi.org/10.1631/jzus.B1600289 Google Scholar
  48. WHO (World Health Organization), 2015. Childbirth: labour, delivery and immediate postpartum care. In: WHO, United Nations Population Fund, UNICEF (Eds.), Pregnancy, Childbirth, Postpartum and Newborn Care: A Guide for Essential Practice, 3rd Ed. World Health Organization, Geneva, p.85–88.Google Scholar
  49. WHO, 2018. Maternal mortality. http://www.who.int/en/newsroom/fact-sheets/detail/maternal-mortality [Accessed on June 4, 2018].Google Scholar
  50. Willenbrock F, Murphy G, 1994. Structure-function relationships in the tissue inhibitors of metalloproteinases. Am J Respir Crit Care Med, 150(6 Pt 2):S165–S170.  https://doi.org/10.1164/ajrccm/150.6_Pt_2.S165 Google Scholar
  51. Wilson PW, Gorny JR, Blackmon WJ, et al., 1986. Fatty acids in the American groundnut (Apios americana). J Food Sci, 51(5):1387–1388.  https://doi.org/10.1111/j.1365-2621.1986.tb13136.x Google Scholar
  52. Woessner JF Jr, 1979. Total, latent and active collagenase during the course of post-partum involution of the rat uterus. Effect of oestradiol. Biochem J, 180(1):95–102.  https://doi.org/10.1042/bj1800095 Google Scholar
  53. Woessner JF Jr, 1996. Regulation of matrilysin in the rat uterus. Biochem Cell Biol, 74(6):777–784.  https://doi.org/10.1139/o96-084 Google Scholar
  54. Wolf K, Sandner P, Kurtz A, et al., 1996. Messenger ribonucleic acid levels of collagenase (MMP-13) and matrilysin (MMP-7) in virgin, pregnant, and postpartum uterus and cervix of rat. Endocrinology, 137(12):5429–5434.  https://doi.org/10.1210/endo.137.12.8940367 Google Scholar
  55. Yan FJ, Yang YY, Yu LS, et al., 2017. Effects of C-glycosides from Apios americana leaves against oxidative stress during hyperglycemia through regulating mitogenactivated protein kinases and nuclear factor erythroid 2-related factor 2. J Agric Food Chem, 65(34):7457–7466.  https://doi.org/10.1021/acs.jafc.7b03163 Google Scholar
  56. Yoshii A, Kitahara S, Ueta H, et al., 2014. Role of uterine contraction in regeneration of the murine postpartum endometrium. Biol Reprod, 91(2):32.  https://doi.org/10.1095/biolreprod.114.117929 Google Scholar
  57. Zhang YZ, Zhou CS, Tang SM, et al., 2011. Effect of AATI, a bowman-birk type inhibitor from Apios americana, on proliferation of cancer cell lines. Food Chem, 128(4):909–915.  https://doi.org/10.1016/j.foodchem.2011.03.117 Google Scholar

Copyright information

© Zhejiang University and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Biosystems Engineering and Food ScienceZhejiang UniversityHangzhouChina
  2. 2.National Engineering Laboratory of Intelligent Food Technology and EquipmentHangzhouChina
  3. 3.Zhejiang Key Laboratory for Agro-Food ProcessingHangzhouChina
  4. 4.Fuli Institute of Food ScienceHangzhouChina
  5. 5.Women’s Hospital, School of MedicineZhejiang UniversityHangzhouChina

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