The promise of novel treatments for severe chronic neutropenia

References

• Dale DC, Welte K. Williams Hematol. 10th (NY) (NY): McGraw Hill; 2021. Chapter 63, Neutropenia and Neutrophilia. p. 1021–1036
   Google Scholar
• Dale DC, Bolyard AA. An update on the diagnosis and treatment of chronic idiopathic neutropenia. Curr Opin Hematol. 2017 Jan;24(1):46–53. PMID: 27841775; PMCID: PMC5380401. doi: 10.1097/MOH.0000000000000305
   PubMed Web of Science ®Google Scholar
• Dale DC, Bolyard AA, Shannon JA, et al. Outcomes for patients with severe chronic neutropenia treated with granulocyte colony-stimulating factor. Blood Adv. 2022 Jul 12;6(13):3861–3869. PMID: 35476051; PMCID: PMC9278291. doi: 10.1182/bloodadvances.2021005684
   PubMed Web of Science ®Google Scholar
• Bar-Joseph G, Halberthal M, Sweed Y, et al. Clostridium septicum infection in children with cyclic neutropenia. J Pediatr. 1997 Aug;131(2):317–319. PMID: 9290625 doi: 10.1016/s0022-3476(97)70175-6
   PubMed Web of Science ®Google Scholar
• Newburger PE. Autoimmune and other acquired neutropenias. Hematology Am Soc Hematol Educ Program. [2016 Dec 2];2016(1):38–42. PMID: 27913460; PMCID: PMC5380382. doi: 10.1182/asheducation-2016.1.38
   PubMedGoogle Scholar
• Palmblad J, Nilsson CC, Höglund P, et al. How we diagnose and treat neutropenia in adults. Expert Rev Hematol. 2016 May;9(5):479–487. Epub 2016 Feb 16. PMID: 26778239 doi: 10.1586/17474086.2016.1142867
   PubMed Web of Science ®Google Scholar
• Papadaki HA, Pontikoglou C. Pathophysiologic mechanisms, clinical features and treatment of idiopathic neutropenia. Expert Rev Hematol. 2008 Dec;1(2):217–229. PMID: 21082926. doi: 10.1586/17474086.1.2.217
   PubMed Web of Science ®Google Scholar
• Skokowa J, Dale DC, Touw IP, et al. Severe congenital neutropenias. Nat Rev Dis Primers. 2017 Jun 8;3(1):17032. PMID: 28593997; PMCID: PMC5821468. doi: 10.1038/nrdp.2017.32
   PubMedGoogle Scholar
• Dale DC, Makaryan V ELANE-Related Neutropenia. In: Adam, MP, Mirzaa, GM, Pagon, RA, Wallace, SE, Bean, LJH, Gripp, KW, Amemiya A editor. GeneReviews® [Internet] [PMID: 20301705]. Seattle (WA): University of Washington, Seattle; 2002 Jun 17 [[updated 2018 Aug 23]]. p. 1993–2023
   Google Scholar
• Boxer LA, Bolyard AA, Kelley ML, et al. Use of granulocyte colony-stimulating factor during pregnancy in women with chronic neutropenia. Obstet Gynecol. 2015 Jan;125(1):197–203. PMID: 25560125; PMCID: PMC4286310 doi: 10.1097/AOG.0000000000000602
   PubMed Web of Science ®Google Scholar
• Chatta GS, Price TH, Stratton JR, et al. Aging and marrow neutrophil reserves. J Am Geriatr Soc. 1994 Jan;42(1):77–81. PMID: 7506277 doi: 10.1111/j.1532-5415.1994.tb06077.x
   PubMed Web of Science ®Google Scholar
• Steward CG, Groves SJ, Taylor CT, et al. Neutropenia in Barth syndrome: characteristics, risks, and management. Curr Opin Hematol. 2019 Jan;26(1):6–15. PMID: 30451719; PMCID: PMC6392059. doi: 10.1097/MOH.0000000000000472
   PubMed Web of Science ®Google Scholar
• Kishnani PS, Austin SL, Abdenur JE, et al. American College of Medical Genetics and Genomics. Diagnosis and management of glycogen storage disease type I: a practice guideline of the American College of Medical Genetics and Genomics. Genet Med. 2014 Nov;16(11):e1. PMID: 25356975 doi: 10.1038/gim.2014.128
   PubMedGoogle Scholar
• Dale DC, Bolyard AA, Marrero T, et al. Neutropenia in glycogen storage disease Ib: outcomes for patients treated with granulocyte colony-stimulating factor. Curr Opin Hematol. 2019 Jan;26(1):16–21. PMID: 30451720; PMCID: PMC7000169. doi: 10.1097/MOH.0000000000000474
   PubMed Web of Science ®Google Scholar
• Myers KC, Furutani E, Weller E, et al. Clinical features and outcomes of patients with Shwachman-Diamond syndrome and myelodysplastic syndrome or acute myeloid leukaemia: a multicentre, retrospective, cohort study. Lancet Haematol. 2020 Mar;7(3):e238–e246. Epub 2019 Dec 23. PMID: 31879230; PMCID: PMC7984274. doi: 10.1016/S2352-3026(19)30206-6
   PubMed Web of Science ®Google Scholar
• Makaryan V, Zeidler C, Bolyard AA, et al. The diversity of mutations and clinical outcomes for ELANE-associated neutropenia. Curr Opin Hematol. 2015 Jan;22(1):3–11. PMID: 25427142; PMCID: PMC4380169. doi: 10.1097/MOH.0000000000000105
   PubMed Web of Science ®Google Scholar
• Metcalf D. Hematopoietic cytokines. Blood. [2008 Jan 15];111(2):485–491. PMID: 18182579; PMCID: PMC2200848. doi: 10.1182/blood-2007-03-079681
   PubMed Web of Science ®Google Scholar
• Lieschke GJ, Grail D, Hodgson G, et al. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood. 1994 Sep 15;84(6):1737–1746. PMID: 7521686. doi: 10.1182/blood.V84.6.1737.1737
   PubMed Web of Science ®Google Scholar
• Hammond WP, Csiba E, Canin A, et al. Chronic neutropenia. A new canine model induced by human granulocyte colony-stimulating factor. J Clin Invest. 1991 Feb;87(2):704–710. PMID: 1704019; PMCID: PMC296362 doi: 10.1172/JCI115049
   PubMed Web of Science ®Google Scholar
• Dale DC, Lau S, Nash R, et al. Effect of endotoxin on serum granulocyte and granulocyte-macrophage colony-stimulating factor levels in dogs. J Infect Dis. 1992 Apr;165(4):689–694. PMID: 1372636 doi: 10.1093/infdis/165.4.689
   PubMed Web of Science ®Google Scholar
• Price TH, Chatta GS, Dale DC. Effect of recombinant granulocyte colony-stimulating factor on neutrophil kinetics in normal young and elderly humans. Blood. 1996 Jul 1;88(1):335–340. PMID: 8704192. doi: 10.1182/blood.V88.1.335.335
   PubMed Web of Science ®Google Scholar
• Dale DC, Bonilla MA, Davis MW, et al. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood. 1993 May 15;81(10):2496–2502. PMID: 8490166; PMCID: PMC4120868. doi: 10.1182/blood.V81.10.2496.2496
   PubMed Web of Science ®Google Scholar
• Dale DC, Cottle TE, Fier CJ, et al. Severe chronic neutropenia: treatment and follow-up of patients in the severe chronic neutropenia International Registry. Am J Hematol. 2003 Feb;72(2):82–93. PMID: 12555210 doi: 10.1002/ajh.10255
   PubMed Web of Science ®Google Scholar
• Gilman PA, Jackson DP, Guild HG. Congenital agranulocytosis: prolonged survival and terminal acute leukemia. Blood. 1970 Nov;36(5):576–585. PMID: 4319697. doi: 10.1182/blood.V36.5.576.576
   PubMed Web of Science ®Google Scholar
• Souza LM, Boone TC, Gabrilove J, et al. Recombinant human granulocyte colony-stimulating factor: effects on normal and leukemic myeloid cells. Science. 1986 Apr 4;232(4746):61–65. PMID: 2420009.doi: 10.1126/science.232.4746.61
   PubMed Web of Science ®Google Scholar
• Rosenberg PS, Alter BP, Bolyard AA, et al. Severe chronic neutropenia International Registry. The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood. 2006 Jun 15;107(12):4628–4635. Epub 2006 Feb 23. PMID: 16497969; PMCID: PMC1895804. doi: 10.1182/blood-2005-11-4370
   PubMed Web of Science ®Google Scholar
• Rosenberg PS, Zeidler C, Bolyard AA, et al. Stable long-term risk of leukaemia in patients with severe congenital neutropenia maintained on G-CSF therapy. Br J Haematol. 2010 Jul;150(2):196–199. Epub 2010 Apr 29. PMID: 20456363; PMCID: PMC2906693. doi: 10.1111/j.1365-2141.2010.08216.x
   PubMed Web of Science ®Google Scholar
• Dale DC, Rosenberg PS, Alter BP. Lineage-specific hematopoietic growth factors. N Engl J Med. 2006 Aug 3;355(5):526–527. author reply 527. PMID: 16888846.
   PubMedGoogle Scholar
• Deordieva E, Shvets O, Voronin K, et al. Nicotinamide (vitamin B3) treatment improves response to G-CSF in severe congenital neutropenia patients. Br J Haematol. 2021 Feb;192(4):788–792. Epub 2021 Jan 20. PMID: 33471934. doi: 10.1111/bjh.17313
   PubMed Web of Science ®Google Scholar
• Makaryan V, Kelley ML, Fletcher B, et al. Elastase inhibitors as potential therapies for ELANE-associated neutropenia. J Leukocyte Biol. 2017 Oct;102(4):1143–1151. Epub 2017 Jul 28. PMID: 28754797; PMCID: PMC5597518 doi: 10.1189/jlb.5A1016-445R
   PubMed Web of Science ®Google Scholar
• Nasri M, Ritter M, Mir P, et al. CRISPR/Cas9-mediated ELANE knockout enables neutrophilic maturation of primary hematopoietic stem and progenitor cells and induced pluripotent stem cells of severe congenital neutropenia patients. Haematologica. 2020 Mar;105(3):598–609. Epub 2019 Jun 27. PMID: 31248972; PMCID: PMC7049355. doi: 10.3324/haematol.2019.221804
   PubMed Web of Science ®Google Scholar
• Makaryan V, Kelley M, Fletcher B, et al. Comparison of gene editing versus a neutrophil elastase inhibitor as potential therapies for ELANE neutropenia. J Cell Immunol. 2022;4(1):19–28. PMID: 36052149; PMCID: PMC9431957. doi: 10.33696/immunology.4.129
   PubMedGoogle Scholar
• Sabo P, Makaryan V, Dicken Y, et al. Mutant allele knockout with novel CRISPR nuclease promotes myelopoiesis in ELANE neutropenia. Mol Ther methods Clin Dev. Mol Ther Methods Clin Dev. 2022 Jun 9;26:119–131. PMID: 35795780; PMCID: PMC9240714 doi: 10.1016/j.omtm.2022.06.002
   PubMed Web of Science ®Google Scholar
• Heusinkveld LE, Majumdar S, Gao JL, et al. WHIM syndrome: from pathogenesis towards personalized Medicine and cure. J Clin Immunol. 2019 Aug;39(6):532–556. Epub 2019 Jul 16. PMID: 31313072; PMCID: PMC6698215. doi: 10.1007/s10875-019-00665-w
   PubMed Web of Science ®Google Scholar
• Geier CB, Ellison M, Cruz R, et al. Disease Progression of WHIM syndrome in an International cohort of 66 pediatric and adult patients. J Clin Immunol. 2022 Nov;42(8):1748–1765. Epub 2022 Aug 10. PMID: 35947323; PMCID: PMC9700649. doi: 10.1007/s10875-022-01312-7
   PubMed Web of Science ®Google Scholar
• Dale DC, Dick E, Kelley M, et al. Family studies of warts, hypogammaglobulinemia, immunodeficiency, myelokathexis syndrome. Curr Opin Hematol. 2020 Jan;27(1):11–17. PMID: 31652152; PMCID: PMC7241424 doi: 10.1097/MOH.0000000000000554
   PubMed Web of Science ®Google Scholar
• Chen B. Molecular mechanism of HIV-1 entry. Trends Microbiol. 2019 Oct;27(10):878–891. Epub 2019 Jun 28. PMID: 31262533; PMCID: PMC6744290. doi: 10.1016/j.tim.2019.06.002
   PubMed Web of Science ®Google Scholar
• Hernandez PA, Gorlin RJ, Lukens JN, et al. Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat Genet. 2003 May;34(1):70–74. PMID: 12692554. doi: 10.1038/ng1149
   PubMed Web of Science ®Google Scholar
• Hübel K, Liles WC, Broxmeyer HE, et al. Leukocytosis and mobilization of CD34+ hematopoietic progenitor cells by AMD3100, a CXCR4 antagonist. Support Cancer Ther. 2004 Apr 1;1(3):165–172. PMID: 18628138. doi: 10.3816/SCT.2004.n.008
   PubMedGoogle Scholar
• Liles WC, Broxmeyer HE, Rodger E, et al. Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood. [2003 Oct 15];102(8):2728–2730. Epub 2003 Jul 10. PMID: 12855591. doi: 10.1182/blood-2003-02-0663
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Orschell CM, Clapp DW, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med. 2005 Apr 18;201(8):1307–1318. PMID: 15837815; PMCID: PMC2213145. doi: 10.1084/jem.20041385
   PubMed Web of Science ®Google Scholar
• Dale DC, Bolyard AA, Kelley ML, et al. The CXCR4 antagonist plerixafor is a potential therapy for myelokathexis, WHIM syndrome. Blood. [2011 Nov 3];118(18):4963–4966. Epub 2011 Aug 11. PMID: 21835955; PMCID: PMC3673761. doi: 10.1182/blood-2011-06-360586
   PubMed Web of Science ®Google Scholar
• McDermott DH, Pastrana DV, Calvo KR, et al. Plerixafor for the treatment of WHIM syndrome. N Engl J Med. [2019 Jan 10];380(2):163–170. PMID: 30625055; PMCID: PMC6425947. doi: 10.1056/NEJMoa1808575
   PubMed Web of Science ®Google Scholar
• Dale DC, Firkin F, Bolyard AA, et al. Results of a phase 2 trial of an oral CXCR4 antagonist, mavorixafor, for treatment of WHIM syndrome. Blood. 2020 Dec 24;136(26):2994–3003. PMID: 32870250; PMCID: PMC7770568. doi: 10.1182/blood.2020007197
   PubMed Web of Science ®Google Scholar
• Badolato R, Donadieu J, 4WHIM study group. Results of a phase 3 trial of an oral CXCR4 antagonist, mavorixafor, for treatment of patients with WHIM syndrome. European Hematology Association Annual Congress; 2023 Jun 8-15; Frankfurt, Germany.
   Google Scholar
• Dale DC, Treon SP, McDermott DF, et al. Oral administration of mavorixafor, a CXCR4 antagonist, increases peripheral white blood cell counts across different disease states. Blood. 2021;138(Supplement 1):2186. doi: 10.1182/blood-2021-152990
   Google Scholar
• Sim SW, Weinstein DA, Lee YM, et al. Glycogen storage disease type Ib: role of glucose-6-phosphate transporter in cell metabolism and function. FEBS Lett. 2020 Jan;594(1):3–18. Epub 2019 Nov 22. PMID: 31705665 doi: 10.1002/1873-3468.13666
   PubMed Web of Science ®Google Scholar
• Chou JY, Cho JH, Kim GY, et al. Molecular biology and gene therapy for glycogen storage disease type Ib. J Inherit Metab Dis. 2018 Nov;41(6):1007–1014. Epub 2018 Apr 16. PMID: 29663270 doi: 10.1007/s10545-018-0180-5
   PubMed Web of Science ®Google Scholar
• Veiga-da-Cunha M, Wortmann SB, Grünert SC, et al. Treatment of the neutropenia associated with GSD1b and G6PC3 deficiency with SGLT2 inhibitors. Diagnostics. [2023 May 19];13(10):1803. PMID: 37238286; PMCID: PMC10217388. doi: 10.3390/diagnostics13101803
   Web of Science ®Google Scholar
• Nelson A, Myers K. Shwachman-Diamond syndrome. In: Adam M, GlM M, Pagon R, Wallace S, Bean L, Gripp K Amemiya A editors. GeneReviews® [Internet] [PMID: 20301722]. Seattle (WA): University of Washington, Seattle; 2008 Jul 17 [updated 2018 Oct 18]. p. 1993–2023
   Google Scholar
• Ferreira C, Pierre G, Thompson R, et al. Barth syndrome In: Adam M, Mirzaa G, Pagon R, Wallace S, Bean L, Gripp K Amemiya A editors GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 2014 Oct9 updated 2020 Jul 9 p. 1993–2023. PMID: 25299040
   Google Scholar
• Thompson R, Jefferies J, Wang S, et al. Current and future treatment approaches for Barth syndrome. J Inherit Metab Dis. 2022 Jan;45(1):17–28. Epub 2021 Nov 10. PMID: 34713454 doi: 10.1002/jimd.12453
   PubMed Web of Science ®Google Scholar
• Dabner L, Pieles GE, Steward CG, et al. Treatment of Barth syndrome by cardiolipin manipulation (CARDIOMAN) With bezafibrate: protocol for a randomized placebo-controlled pilot trial conducted in the nationally commissioned Barth syndrome service. JMIR Res Protoc. [2021 May 31];10(5):e22533. PMID: 34057417; PMCID: PMC8204243. doi: 10.2196/22533
   PubMed Web of Science ®Google Scholar
• Sabbah HN. Elamipretide for Barth syndrome cardiomyopathy: gradual rebuilding of a failed power grid. Heart Fail Rev. 2022 Sep;27(5):1911–1923. Epub 2021 Oct 8. PMID: 34623544; PMCID: PMC9388406. doi: 10.1007/s10741-021-10177-8
   PubMed Web of Science ®Google Scholar
• Kohn LA, Kohn DB. Gene therapies for primary immune deficiencies. Front Immunol. 2021 Feb 25;12:648951. PMID: 33717203; PMCID: PMC7946985 doi: 10.3389/fimmu.2021.648951
   PubMed Web of Science ®Google Scholar
• Clinicaltrials.Gov [Internet]. Bethesda MD: National Library of Medicine 2000 Feb 29 [updated 2023 Jul 10-20]. Available from: http://www.clinicaltrials.gov
   Google Scholar