Autophagic vacuolar myopathies: what we have learned from the differential diagnosis of vacuoles in muscle biopsy

Česká verze

Authors: Josef Zámečník; Robert Artur Dahmen
Authors place of work: Ústav patologie a molekulární medicíny, 2. LF UK a FN Motol, Praha
Published in the journal: Čes.-slov. Patol., 49, 2013, No. 1, p. 39-45
Category: Původní práce

Summary

Establishing the correct etiological diagnosis of autophagic vacuolar myopathies (AVM) is an imperative since the recent availability of the enzyme replacement therapy for the treatment of Pompe disease. Recent recognition of the complex functional pathology of these disorders dramatically changed the view on their pathogenesis and it may lead to identification of new approaches in the therapy. Muscle biopsy is a useful tool for the differential diagnosis of the AVM; however, in some cases it may fail.

Through a series of five short case studies we aim at demonstrating the histopathological findings and differential diagnosis of some AVM (Pompe disease, Danon disease and chloroquine myopathy) in muscle biopsy. We also want to address the fact that the way to the correct diagnosis of these disorders can be quite complicated.

Awareness of these diseases and the availability of a dry blood spot test for the non-invasive diagnosis of Pompe disease represent a good basis for detecting patients who are still kept under other diagnoses and thus escaping treatment.

Keywords:
autophagic myopathies – vacuoles – Pompe disease – Danon disease – chloroquine myopathy

Zdroje

1. Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med 2003; 9(3–4): 65–76.

2. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306(5698): 990–995.

3. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21(22): 2861-2873.

4. Raben N, Shea L, Hill V, Plotz P. Monitoring autophagy in lysosomal storage disorders. Methods Enzymol 2009; 453: 417–449.

5. Ballabio A, Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim Biophys Acta 2009; 1793(4): 684–696.

6. Chu CT. Autophagic stress in neuronal injury and disease. J Neuropathol Exp Neurol 2006; 65(5): 423–432.

7. Kurz T, Terman A, Gustafsson B, Brunk UT. Lysosomes and oxidative stress in aging and apoptosis. Biochim Biophys Acta 2008; 1780(11): 1291–1303.

8. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15(3): 1101–1111.

9. Amalfitano A, Bengur AR, Morse RP et al. Recombinant human acid alpha-glucosidase enzyme therapy for infantile glycogen storage disease type II: results of a phase I/II clinical trial. Genet Med 2001; 3(2): 132–138.

10. Pompe J. Over idiopatische hypertrophie van het hart. Ned Tijdshr Geneeskd 1932; 76: 304-312.

11. Di RM, Buzzi D, Taro M. Glycogen storage disease type II: clinical overview. Acta Myol 2007; 26(1): 42–44.

12. Kroos M, Hoogeveen-Westerveld M, van der PA, Reuser AJ. The genotype-phenotype correlation in Pompe disease. Am J Med Genet C Semin Med Genet 2012; 160(1): 59–68.

13. Kroos MA, Pomponio RJ, Hagemans ML et al. Broad spectrum of Pompe disease in patients with the same c.-32-13T->G haplotype. Neurology 2007; 68(2): 110–115.

14. Malinová V. Glykogenóza II. typu (GSD II, m. Pompe). Současné možnosti diagnostiky a terapie. Klinická kazuistika. Neurol prax 2010; 11(5): 326–330.

15. Ausems MG, Verbiest J, Hermans MP et al. Frequency of glycogen storage disease type II in The Netherlands: implications for diagnosis and genetic counselling. Eur J Hum Genet 1999; 7(6): 713–716.

16. Martiniuk F, Chen A, Mack A et al. Carrier frequency for glycogen storage disease type II in New York and estimates of affected individuals born with the disease. Am J Med Genet 1998; 79(1): 69–72.

17. Burton BK. Newborn screening for Pompe disease: an update, 2011. Am J Med Genet C Semin Med Genet 2012; 160(1): 8–12.

18. Chien YH, Lee NC, Huang HJ, Thurberg BL, Tsai FJ, Hwu WL. Later-onset Pompe disease: early detection and early treatment initiation enabled by newborn screening. J Pediatr 2011; 158(6): 1023–1027.

19. Fukuda T, Ewan L, Bauer M et al. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann Neurol 2006; 59(4): 700–708.

20. Kishnani PS, Corzo D, Nicolino M et al. Recombinant human acid [alpha]-glucosidase: major clinical benefits in infantile-onset Pompe disease. Neurology 2007; 68(2): 99–109.

21. Van der Ploeg AT, Clemens PR, Corzo D et al. A randomized study of alglucosidase alfa in late-onset Pompe’s disease. N Engl J Med 2010; 362(15): 1396–1406.

22. Reuser AJ. Enzyme therapy in Pompe disease: questions remain. Mol Genet Metab 2012; 107 (3): 485-489.

23. Nicolino M, Byrne B, Wraith JE et al. Clinical outcomes after long-term treatment with alglucosidase alfa in infants and children with advanced Pompe disease. Genet Med 2009; 11(3): 210–219.

24. Raben N, Jatkar T, Lee A et al. Glycogen stored in skeletal but not in cardiac muscle in acid alpha-glucosidase mutant (Pompe) mice is highly resistant to transgene-encoded human enzyme. Mol Ther 2002; 6(5): 601–608.

25. Raben N, Wong A, Ralston E, Myerowitz R. Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C Semin Med Genet 2012; 160(1): 13–21.

26. Kishnani PS, Goldenberg PC, DeArmey SL et al. Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab 2010; 99(1): 26–33.

27. Zhu Y, Jiang JL, Gumlaw NK et al. Glycoengineered acid alpha-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of Pompe disease. Mol Ther 2009; 17(6): 954–963.

28. Parenti G. Treating lysosomal storage diseases with pharmacological chaperones: from concept to clinics. EMBO Mol Med 2009; 1(5): 268– 279.

29. Laforet P, Petiot P, Nicolino M et al. Dilative arteriopathy and basilar artery dolichoectasia complicating late-onset Pompe disease. Neurology 2008; 70(22): 2063–2066.

30. Sacconi S, Bocquet JD, Chanalet S, Tanant V, Salviati L, Desnuelle C. Abnormalities of cerebral arteries are frequent in patients with late-onset Pompe disease. J Neurol 2010; 257(10): 1730–1733.

31. Nishino I, Fu J, Tanji K et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 2000; 406(6798): 906–910.

32. Tanaka Y, Guhde G, Suter A et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000; 406(6798): 902–906.

33. Nishino I. Autophagic vacuolar myopathies. Curr Neurol Neurosci Rep 2003; 3(1): 64–69.

34. Danon MJ, Oh SJ, DiMauro S et al. Lysosomal glycogen storage disease with normal acid maltase. Neurology 1981; 31(1): 51–57.

35. Sugie K, Yamamoto A, Murayama K et al. Clinicopathological features of genetically confirmed Danon disease. Neurology 2002; 58(12): 1773–1778.

36. Schorderet DF, Cottet S, Lobrinus JA, Borruat FX, Balmer A, Munier FL. Retinopathy in Danon disease. Arch Ophthalmol 2007; 125(2): 231–236.

37. Sugie K, Noguchi S, Kozuka Y et al. Autophagic vacuoles with sarcolemmal features delineate Danon disease and related myopathies. J Neuropathol Exp Neurol 2005; 64(6): 513 –522.

38. Gilman AL, Chan KW, Mogul A et al. Hydroxychloroquine for the treatment of chronic graft-versus-host disease. Biol Blood Marrow Transplant 2000; 6(3A): 327–334.

39. Goldman FD, Gilman AL, Hollenback C, Kato RM, Premack BA, Rawlings DJ. Hydroxychloroquine inhibits calcium signals in T cells: a new mechanism to explain its immunomodulatory properties. Blood 2000; 95(11): 3460–3466.

40. Fox RI, Kang HI. Mechanism of action of antimalarial drugs: inhibition of antigen processing and presentation. Lupus 1993; 2(Suppl 1): 9–12.

41. Schultz KR, Su WN, Hsiao CC et al. Chloroquine prevention of murine MHC-disparate acute graft-versus-host disease correlates with inhibition of splenic response to CpG oligodeoxynucleotides and alterations in T-cell cytokine production. Biol Blood Marrow Transplant 2002; 8(12): 648–655.

42. Bondeson J, Sundler R. Antimalarial drugs inhibit phospholipase A2 activation and induction of interleukin 1beta and tumor necrosis factor alpha in macrophages: implications for their mode of action in rheumatoid arthritis. Gen Pharmacol 1998; 30(3): 357–366.

43. McChesney EW. Animal toxicity and pharmacokinetics of hydroxychloroquine sulfate. Am J Med 1983; 75(1A): 11–18.

44. Sundelin SP, Terman A. Different effects of chloroquine and hydroxychloroquine on lysosomal function in cultured retinal pigment epithelial cells. APMIS 2002; 110(6): 481–489.

45. Bolanos-Meade J, Zhou L, Hoke A, Corse A, Vogelsang G, Wagner KR. Hydroxychloroquine causes severe vacuolar myopathy in a patient with chronic graft-versus-host disease. Am J Hematol 2005; 78(4): 306–309.

46. Zámečník J, Veselý D, Jakubička B et al. Atrophy of type II fibres in myasthenia gravis muscle in thymectomized patients: steroid-induced change with prognostic impact. J Cell Mol Med 2009; 13(8B): 2008–2018.

47. Zámečník J, Veselý D, Jakubička B et al. Muscle lymphocytic infiltrates in thymoma-associated myasthenia gravis are phenotypically different from those in polymyositis. Neuromuscul Disord 2007; 17(11–12): 935–942.

48. Kuncová K, Sedláčková M, Vencovský J, Mann H, Wenchich L, Zámečník J. Inflammatory myopathy associated with statins: Report of 3 Cases. Mod Rheumatol 2013; in press.