490
Views
13
CrossRef citations to date
0
Altmetric
Review

Leukemia and male infertility: past, present, and future

ORCID Icon, , &
Pages 1126-1135 | Received 26 Apr 2018, Accepted 30 Sep 2018, Published online: 03 Dec 2018

References

  • Huleihel M. Spermatogenesis in an artificial three-dimensional system. Stem cells. 2012;30:2355–2360.
  • Huleihel M, Abuelhija M, Lunenfeld E. In vitro culture of testicular germ cells: regulatory factors and limitations. Growth Factors. 2007; 25:236–252.
  • Huleihel M, Nourashrafeddin S, Plant TM. Application of three-dimensional culture systems to study mammalian spermatogenesis, with an emphasis on the rhesus monkey (Macaca mulatta). Asian J Androl. 2015;17:972–980.
  • Plant TM, Marshall GR. The functional significance of FSH in spermatogenesis and the control of its secretion in male primates. Endocr Rev. 2001;22:764–786.
  • França LR, Hess RA, Dufour JM, et al. The Sertoli cell: one hundred fifty years of beauty and plasticity. Andrology. 2016;4:189–212.
  • de Kretser DM, Loveland KL, Meinhardt A, et al. Spermatogenesis. Hum Reprod. 1998;13:1–8.
  • Loveland KL, Klein B, Puesch D, et al. Cytokines in male fertility and reproductive pathologies: immunoregulation and beyond. Front Endocrinol. 2017;8:1–16.
  • Potter SJ, DeFalco T. Role of the testis interstitial compartment in spermatogonial stem cell function. Reproduction. 2017;153:R151–R162.
  • Weinbauer GF, Luetjens CM, Simoni M, et al. Physiology of testicular function. In: Nieschlag E Behre H.M., Nieschlag S. (eds) Andrology. Berlin, Heidelberg: Springer; 2008:11–59.
  • Akhtar M, Ali MA, Burgess A, et al. Fine-needle aspiration biopsy (FNAB) diagnosis of testicular involvement in acute lymphoblastic leukemia in children. Diagn Cytopathol. 1991;7:504–507.
  • Kobayashi H, Urashima M, Hoshi Y, et al. Testicular morphological changes in children with acute lymphoblastic leukemia following chemotherapy. Acta Paediatr JPN. 1996;38:640–643.
  • Ishigami K, Yousef-Zahra DM, Abu-Yousef MM. Enlargement and hypervascularity of both the epididymis and testis do not exclude involvement with lymphoma or leukemia. J Clin Ultrasound. 2004;32:365–369.
  • Krawczuk-Rybak M, Płonowski M, Solarz E, et al. Assessment of gonadal function in boys and adolescents at the diagnosis of neoplastic disease. J Pediatr Endocrinol Metab. 2012;25:453–458.
  • Krawczuk-Rybak M, Solarz E, Wołczyński S. Male gonadal function before and after chemotherapy in prepubertal boys. Roczniki Akademii Medycznej W Bialymstoku. 2004;49:126–128.
  • Ward E, DeSantis C, Robbins A, et al. Childhood and adolescent cancer statistics, 2014. CA Cancer J Clin. 2014;64:83–103.
  • Moore AS, Kearns PR, Knapper S, et al. Novel therapies for children with acute myeloid leukaemia. Leukemia. 2013;27:1451–1460.
  • Fraumeni JF, Hoover RN, Devesa SS, et al. Epidemiology of cancer. In: DeVita VT, Hellman S, Rosenberg SA, editors. Cancer: principles and practice of oncology. 4th edition. Philadelphia: J.B. Lippincott Co., 1993:150–165.
  • Kreuser ED, Hetzel WD, Heit W, et al. Reproductive and endocrine gonadal functions in adults following multidrug chemotherapy for acute lymphoblastic or undifferentiated leukemia. J Clin Oncol. 1988;6:588–595.
  • Chatterjee R, Goldstone AH. Gonadal damage and effects on fertility in adult patients with haematological malignancy undergoing stem cell transplantation. Bone Marrow Transplant. 1996;17:5–11.
  • van Casteren NJ, van der Linden GH, Hakvoort-Cammel FG, et al. Effect of childhood cancer treatment on fertility markers in adult male long-term survivors. Pediatr Blood Cancer. 2009;52:108–112.
  • Hewitt M, Weiner SL, Simone JV. Childhood cancer survivorship: improving care and quality of life. Washington, D.C: The National Academies Press; 2003.
  • Gassei K, Orwig KE. Experimental methods to preserve male fertility and treat male factor infertility. Fertil Steril. 2016;105:256–266.
  • Jahnukainen K, Mitchell RT, Stukenborg JB. Testicular function and fertility preservation after treatment for hematological cancer. Curr Opin Endocrinol Diab Obes. 2015;22:217–223.
  • Wyns C, Curaba M, Vanabelle B, Van Langendonckt A, Donnez J. Options for fertility preservation in prepubertal boys. Hum Reprod Update. 2010;16:312–328.
  • Chapman RM, Sutcliffe SB, Malpas JS. Male gonadal dysfunction in Hodgkin disease. A prospective study. JAMA. 1981;245:1323–1328.
  • Rueffer U, Breuer K, Josting A, et al. Male gonadal dysfunction in patients with Hodgkin disease prior to treatment. Ann Oncol. 2001;12:1307–1311.
  • Hallak J, Kolettis PN, Sekhon VS, et al. Sperm cryopreservation in patients with testicular cancer. Urology. 1999;54:894–899.
  • Berthelsen JG, Skakkebaek NE. Gonadal function in men with testis cancer. Fertil Steril. 1983;39:68–75.
  • Puscheck E, Philip PA, Jeyendran RS. Male fertility preservation and cancer treatment. Cancer Treat Rev. 2004;30:173–180.
  • (a) Byrne J, Mulvihill JJ, Myers MH, et al. Effects of treatment on fertility in long-term survivors of childhood or adolescent cancer. N Engl J Med. 1987;317:1315–1321. (b) Hamish W, Wallace B. Oncofertility and preservation of reproductive capacity in children and young adults. Cancer. 2011;117:2301–2310.
  • Desandes E. Survival from adolescent cancer. Cancer Treat Rev. 2007;33:609–615.
  • Hudson MM. Reproductive outcomes for survivors of childhood cancer. Obstet Gynecol. 2010;116:1171–1183.
  • Hagenäs I, Jørgensen N, Rechnitzer C, et al. Clinical and biochemical correlates of successful semen collection for cryopreservation from 12–18-year-old patients: a single-center study of 86 adolescents. Hum Reprod. 2010;25:2031–2038.
  • Rofeim O, Gilbert BR. Normal semen parameters in cancer patients presenting for cryopreservation before gonadotoxic therapy. Fertil Steril. 2004;82:505–506.
  • Chung K, Irani J, Knee G, et al. Sperm cryopreservation for male patients with cancer: an epidemiological analysis at the University of Pennsylvania. Eur J Obstet Gynecol Reprod Biol. 2004;113:S7–S11.
  • Auger J, Sermondade N, Eustache F. Semen quality of 4480 young cancer and systemic disease patients: baseline data and clinical considerations. Basic Clin Androl. 2016;26:3.
  • Hotaling JM, Lopushnyan NA, Davenport M, et al. Raw and test-thaw semen parameters after cryopreservation among men with newly diagnosed cancer. Fertil Steril. 2013;99:464–469.
  • Ku JY, Park NC, Jeon TG, et al. Semen analysis in cancer patients referred for sperm cryopreservation before chemotherapy over a 15-year period in Korea. World J Mens Health. 2015;33:8–13.
  • Hallak J, Kolettis PN, Sekhon VS, et al. Cryopreservation of sperm from patients with leukemia: is it worth the effort? Cancer. 1999;85:1973–1978.
  • Johnson MD, Cooper AR, Jungheim ES, et al. Sperm banking for fertility preservation: a 20-year experience. Eur J Obstet Gynecol Reprod Biol. 2013;170:177–182.
  • Nicolini FE, Alcazer V, Huguet F, et al. CML patients show sperm alterations at diagnosis that are not improved with imatinib treatment. Leuk Res. 2016;48:80–83.
  • Agarwal A, Allamaneni SS. Disruption of spermatogenesis by the cancer disease process. J Natl Cancer Inst Monogr. 2005;2005:9–12.
  • Meirow D, Schenker JG. Cancer and male infertility. Hum Reprod. 1995;10:2017–2022.
  • Wang C, McDonald V, Leung A, et al. Effect of increased scrotal temperature on sperm production in normal men. Fertil Steril. 1997;68:334–339.
  • Richie JP. Neoplasms of the testis. In: Walch PC, Retik AB, Vaughan ED, editors. Campbell’s urology. 7th edn. Philadelphia: Saunders; 1998. p 2411.
  • Yuceturk CN, Ozgur BC, Sarici H, et al. Report of an unusual case: testicular involvement of chronic myeloid leukemia 10 years after the complete response. J Clin Diagn Res. 2014;8:ND03–ND04.
  • Pierik FH, Vreeburg JT, Stijnen T, et al. Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab. 1998;83:3110–3114.
  • Meachem SJ, Nieschlag E, Simoni M. Inhibin B in male reproduction: pathophysiology and clinical relevance. Eur J Endocrinol. 2001;145:561–571.
  • Wigny KM, van Dorp W, van der Kooi AL, et al. Gonadal function in boys with newly diagnosed cancer before the start of treatment. Hum Reprod. 2016;31:2613–2618.
  • van Casteren NJ, Boellaard WP, Romijn JC, et al. Gonadal dysfunction in male cancer patients before cytotoxic treatment. Int J Androl. 2010;33:73–79.
  • Crofton PM, Thomson AB, Evans AE, et al. Is inhibin B a potential marker of gonadotoxicity in prepubertal children treated for cancer? Clin Endocrinol (Oxf). 2003;58:296–301.
  • Niemi M, Sharpe RM, Brown WRA. Macrophages in the interstitial tissue of the rat testis. Cell Tissue Res. 1986;243:337–344.
  • Winnall WR, Hedger MP. Phenotypic and functional heterogeneity of the testicular macrophage population: a new regulatory model. J Reprod Immunol. 2013;97:147–158.
  • Locati M, Mantovani A, Sica A. Macrophage activation and polarization as an adaptive component of innate immunity. Adv Immunol. 2013;120:163–184.
  • Gordon S, Plüddemann A. Tissue macrophages: heterogeneity and functions. BMC Biol. 2017;15:53.
  • Bhushan S, Meinhardt A. The macrophages in testis function. J Reprod Immunol. 2017;119:107–112.
  • Bhushan SS, Tchatalbachev Y, Lu S, et al. Differential activation of inflammatory pathways in testicular macrophages provides a rationale for their subdued inflammatory capacity. JI. 2015;194:5455–5464.
  • Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8:958–969.
  • Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451–483.
  • Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13.
  • Lysiak JJ, Nguyen QAT, Kirby JL, et al. Ischemia-reperfusion of the murine testis stimulates the expression of proinflammatory cytokines and activation of c-jun N-terminal kinase in a pathway to E-selectin expression. Biol Reprod. 2003;69:202–210.
  • Turner TT, Brown KJ. Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol Reprod. 1993;49:401–407.
  • Turner TT, Tung KSK, Tomomasa H, et al. Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol Reprod. 1997;57:1267–1274.
  • Lysiak JJ, Turner SD, Nguyen QAT, et al. Essential role of neutrophils in germ cell-specifc apoptosis following ischemia/reperfusion injury of the mouse testis. Biol Reprod. 2001;65:718–725.
  • Frungieri MB, Calandra RS, Lustig L, et al. Macrophages in the testis of infertile men: number, distribution pattern and identification of expressed genes by laser-microdissection and RT-PCR analysis. Fertil Steril. 2002;78:298–306.
  • Białas M, Fiszer D, Rozwadowska N, et al. The role of IL-6, IL-10, TNF-alpha and its receptors TNFR1 and TNFR2 in the local regulatory system of normal and impaired human spermatogenesis. Am J Reprod Immunol. 2009;62:51–59.
  • Disis ML. Immune regulation of cancer. J Clin Oncol. 2010;28:4531–4538.(b)Ganaiem M, AbuElhija M, Lunenfeld E, et al. Effect of interleukin-1 receptor antagonist gene deletion on male mouse fertility. Endocrinology. 2009;150:295–303.
  • Abu Elheija M, Dyomin V, Ganaiem M, et al. Distinct expression of interleukin-1α, interleukin-1β, and interleukin-1 receptor antagonist in testicular tissues and cells from human biopsies with normal and abnormal histology. J Interferon Cytokine Res. 2011;31:401–408.
  • Elhija MA1, Lunenfeld E, Huleihel M. Induction of IL-1, in the testes of adult mice, following subcutaneous administration of turpentine. Am J Reprod Immunol. 2006;55:136–144.
  • Elhija MA1, Potashnik H, Lunenfeld E, et al. Testicular interleukin-6 response to systemic inflammation. Eur Cytokine Netw. 2005;16:167–172.
  • Landskron G, De la Fuente M, Thuwajit P, et al. Chronic inflammation and cytokines in the tumour microenvironment. J Immunol Res. 2014;2014:1.
  • van Etten RA. Aberrant cytokine signaling in leukemia. Oncogene. 2007;26:6738–6749.
  • Hsu HC, Lee YM, Tsai WH, et al. Circulating levels of thrombopoietic and inflammatory cytokines in patients with acute myeloblastic leukemia and myelodysplastic syndrome. Oncology. 2002;63:64–69.
  • Dokter WH, Tuyt L, Sierdsema SJ, et al. The spontaneous expression of interleukin-1 beta and interleukin-6 is associated with spontaneous expression of AP-1 and NF-kappa B transcription factor in acute myeloblastic leukemia cells. Leukemia. 1995;9:425–432.
  • Griffin JD, Rambaldi A, Vellenga E, et al. Secretion of interleukin-1 by acute myeloblastic leukemia cells in vitro induces endothelial cells to secrete colony stimulating factors. Blood. 1987;70:1218–1221.
  • Birkenkamp KU, Esselink MT, Kruijer W, et al. Differential effects of interleukin-3 and interleukin-1 on the proliferation and interleukin- 6 protein secretion of acute myeloid leukemic cells; the involvement of ERK, p38 and STAT5. Eur Cytokine Netw. 1999;10:479–490.
  • Huleihel M, Lunenfeld E, Blindman A, et al. Over expression of interleukin-1alpha, interleukin-1beta and interleukin-1 receptor antagonist in testicular tissues from sexually immature mice as compared to adult mice. Eur Cytokine Netw. 2003;14:27–33.
  • Huleihel M, Lunenfeld E. Involvement of intratesticular IL-1 system in the regulation of Sertoli cell functions. Mol Cell Endocrinol. 2002;187:125–132.
  • Huleihel M, Zeyse D, Lunenfeld E, et al. Induction of transferrin secretion in murine Sertoli cells by FSH and IL-1: the possibility of different mechanism(s) of regulation. Am J Reprod Immunol. 2002; 47:112–117.
  • Zeyse D, Lunenfeld E, Beck M, et al. Induction of interleukin-1alpha production in murine Sertoli cells by interleukin-1. Biol Reprod. 2000;62:1291–1296. (b) Zeyse D, Lunenfeld E, Beck M, et al. Interleukin-1 receptor antagonist is produced by sertoli cells in v. Endocrinology. 2000;141:1521–1527
  • Piquet-Pellorce C, Dorval I, Jégou B. Paracrine control of spermatogenetic stem cells: example of the leukemia inhibitory factor. Contracept Fertil Sex. 1997;25:565–568.
  • Matsui Y, Toksoz D, Nishikawa S, et al. Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature. 1991;353:750–752.
  • Pesce M, Farrace MG, Piacentini M, et al. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development. 1993;118:1089–1094.
  • Mauduit C, Hamamah S, Benahmed M. Stem cell factor/c-kit system in spermatogenesis. Contracept Fertil Sex. 1999;27:735–742.
  • Rossi P, Sette C, Dolci S, et al. Role of c-kit in mammalian spermatogenesis. J Endocrinol Invest. 2000;23:609–615.
  • Tadokoro Y, Yomogida K, Ohta H, et al. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev. 2002;113:29–39.
  • Hofmann MC, Braydich-Stolle L, Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol. 2005;279:114–124.
  • Yomogida K, Yagura Y, Tadokoro Y, et al. Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells. Biol Reprod. 2003;69:1303–1307.
  • Huleihel M, Fadlon E, Abuelhija A, et al. Glial cell line-derived neurotrophic factor (GDNF) induced migration of spermatogonial cells in vitro via MEK and NF-kB pathways. Differentiation. 2013;86:38–47.
  • Meinhardt A, Bacher M, McFarlane JR, et al. Macrophage migration inhibitory factor production by Leydig cells: evidence for a role in the regulation of testicular function. Endocrinology. 1996;137:5090–5095.
  • Meinhardt A, Bacher M, Wennemuth G, et al. Macro phage migration inhibitory factor (MIF) as a paracrine mediator in the interaction of testicular somatic cells. Andrologia. 2000;32:46–48.
  • Wennemuth G, Aumüller G, Bacher M, et al. Macrophage migration inhibitory factor-induced Ca(2+) response in rat testicular peritubular cells. Biol Reprod. 2000;62:1632–1639.
  • Huleihel M, Abofoul-Azab M, Abarbanel Y, et al. Production of macrophage inhibitory factor (mif) by primary Sertoli cells; its possible involvement in migration of spermatogonial cells. J Cell Physiol. 2017;232:2869–2877.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.