sarcolemmal coexpression of intercellular adhesion molecule-1 (icam-1) and hla-dr in inflammatory...

Neuropathology 14 : 149-157, 1994

Original Article

Sarcolemmal Coexpression of Intercellular Adhesion Molecule- 1 (ICAM- 1) and HLA-DR

in Inflammatory Myopathy

Jun Shimizu, Mitsuru Kawai and Ichiro Kanazawa

Department of Neurology, Institute for Brain Research, School of Medicine, University of Tokyo

(Received Octorber 21, 1994 ; Revised and Accepted December 12,1994)

This report concerns the immunohistochemical detec- tion of the intercellular adhesion molecule-1 (ICAM-l), HLA-ABC and HLA-DR in consecutive cryostat sections of skeletal muscle biopsies from 38 patients with inflammatory myopathy. Among these were 12 cases of dermatomyositis, 22 cases of polymyositis, two cases each of inclusion body myositis and sarcoid myopathy. Speci- mens from eight cases of Duchenne muscular dystrophy, three cases each of alcoholic polyneuropathy and myotonic dystrophy, two cases of motor neuron disease, and three normal individuals were included for comparison. Sarco- lemma1 ICAM-1 expression by undamaged muscle fibers was detected in 18/38 cases of inflammatory myopathy who had large numbers of endomysial inflammatory cells, but not in normals or patients with non-inflammatory myopathy. Sarcolemmal immunostaining was more intense in the vicinity of the inflammatory cells. Some regenerating muscle fibers, irrespective of disease, expressed sarcoplasmic ICAM-1. Sarcolemmal HLA- ABC and HLA-DR immunoreactivity was detected in undamaged muscle fibers of 37/38 and 18/38 cases of inflammatory myopathy, respectively. Sarcolemmal immunostaining for HLA-DR was observed in cases with large amounts of endomysial inflammatory cells, and was stronger in muscle fibers that were in their vicinity. HLA-DR and ICAM-1 immunoreaction product deposits were generally colocalized in the sarcolemma of the same fibers. The specific sarcolemmal expression of ICAM-1, and its colocalization with HLA-DR may be important for the recognition of muscle fibers by invading inflammatory cells in inflammatory myopathy.

Key words : HLA-ABC, HLA-DR, ICAM-1, Immuno- histochemistry, Inflammatory myopathy, Muscle.

Introduction

It has recently been demonstrated that cell adhesion molecules have an important role in the immune

response by mediating cell-cell interactions. The for- mation of conjugates between T cells and antigen- presenting cells is a prerequisite for antigen-specific T cell activation. The interaction between several distinct receptors and ligands in cells of the immune system is involved in T cell activation by antigen- presenting or target cells. Thus, the reactions of HLA-ABC and HLA-DR molecules on antigen- presenting cells in conjugation with presentation of processed exogenous antigens, and their respective ligands, CD8 and CD4 on T lymphocytes, are antigen- restricted interactions. The aberrant expression of HLA-ABC, HLA-DR, or other adhesion molecules has been described in various tissues, including skeletal muscle and rejected tissue allografts3~21*29,38~44. More- over, lymphocyte-function associated antigen- l (LFA- 1)IICAM-1 and CD2/LFA-3 are other non-antigen- restricted receptor/ligand pairs that are essential for the interaction of T cells and target cells.

The binding of ICAM-I, a cell adhesion molecule and member of the immunoglobulin superfamily and its ligand, LFA-1, is a key initial step in many im- munologic and inflammatory processes, and the impor- tance of this receptor/ligand pair has been documented in a variety of s t ~ d i e s ' ~ , ~ ~ , ~ ~ . Antibodies to adhesion molecules block leukocyte and lymphocyte interactions, and inhibit certain lymphocyte functions that include cytotoxicity and proliferation in mixed lymphocyte cultures, while antibodies to LFA- 1 pre- vent graft rejection in vivo. ICAM-I is expressed by vascular endothelial cells, dendritic cells, fibroblast- like cells and some epithelial cells of normal tis- s u e ~ " , ~ ~ , whereas its aberrant expression has been reported in several autoimmune diseases9~17~31*45~48~52 and in rejected tissue allograft^'*^^'^*^^. However, there are few data on ICAM-1 expression in normal skeletal

150 Neuropathology 14, 1994

muscle and in muscle from patients with various d i s e a ~ e ~ , ~ ~ , and there is almost no information on the distribution of ICAM-1 in muscle fibers in primary and secondary inflammation.

The aim of the present investigation is to delineate expression and distribution of ICAM-1 in muscles from individuals with various neuromuscular disorders, including inflammatory myopathy, and to determine the relationship between ICAM-1 expression and HLA-ABC and HLA-DR expression in inflammatory myopathy.

Materials and Method

This study was carried on specimens from 38 patients with inflammatory myopathy. Of these, 12 had dermatomyositis (DM) ; 22, polymyositis (PM) ; two, inclusion body myositis (IBM); and two, sarcoid myopathy. In addition, we also examined samples from eight patients with Duchenne muscular dystrophy (DMD), three each with myotonic dystrophy and alcoholic polyneuropathy, and two with motor neuron disease (MND). Three normal control individuals with no microscopi- cally evident abnormality were also included in the study. The DM and PM diagnoses were based on the criteria of Bohan et

Although cases 2, 3 and 4 had no inflammatory cells in their biopsied specimens, these patients had typical D M skin changes and symmetric muscle weakness, increased serum creatine kinase levels, and electromyographic changes characteristic of myositis. Cases 1 and 5 to 34 met the criteria of “definite” PM or DM. The skeletal muscle (biceps, deltoid, quadriceps, gastrocnemius, tibialis anterior) specimens, obtained by biopsy were rapidly frozen in chilled isopentane and stored at -880°C until use. Consecutive 8 p m sections were stained with hematoxylin-eosin (H&E), and assayed histochemically for myosin ATPase and acid phosphatase. Sections stained with monoclonal antibodies against inflammatory cells were also used to identify these cells.

The following antibodies (dilutions and suppliers in parenth- eses) were used for the immunohistochemical tests : Two monoclonal antibodies against ICAM-1 (CD54), RR1/1, (1 : 100) (Bender Medsystems), and BBA3 (1 : 1,000) (British Biotech- nology) ; a monoclonal antibody to HLA-ABC, PHM4 (1 : 100) (Australian Monoclonal Development) ; two monoclonal antibodies against HLA-DR, LN3 ( 1 : 5) ( N i ~ h i r e i ) ’ ~ , ~ ~ , and L243 (1 : 10) (Becton D i c k i n s ~ n ) ~ ~ , and monoclonal antibodies against CD20 (B cell), L26 (1 : 50) ; CD45 (T cell), VCHLI (1 : 50) ; CD64 (macrophage) ( 1 : 100) (Dakopatts). After fixation in cold acetone for 10 rnin, the sections were rinsed with Tris- buffered saline (TBS), preincubated for 30 min with 10% normal goat serum, and then incubated with primary antibodies for 2 h. Antibody binding was visualized by the avidin-biotin-immunoperoxidase complex (ABC) method ; 3, 3’ diaminoben- zidine tetrahydrochloride (DAB) was the final chromogen. The proportion of inflammatory cells identified by H&E staining, acid-phosphatase activity and immunohistochemical staining was evaluated semiquantitatively using a - to # scale, where- =absent or sparse ; + =small amount ; + =moderate amount ; # =large amount of inflammatory cells.

Results

H&E and immunohistochernical staining for inflammatory cells

There was a tendency for the infiltration by inflammatory cells to be predominantly perimysial in the DM cases, and mostly endomysial in the PM patients. Perifascicular atrophy was observed in the specimens from cases 8,9, 10,27, 33 and 34. Although perifascicular atrophy is considered to be a typical finding in DM, cases 9 and 33 lacked the characteristic skin changes. The immunohistochemical tests for inflammatory cells provided data on the distribution and number of CD20-positive (B cell), CD45-positive (T cell), and CD68-positive (macrophage) cells in the sections. The results indicated that T cells and macrophages were abundant and B cells, sparse in the endomysium of PM patients. On the other hand, B cells, T cells and macrophages were abundant in the perimysial or perivascular spaces of the patients with DM. The mononuclear cells in non-necrotic muscle fibers present in the specimens of two PM patients (cases 28 and 29) were CD45-positive T cells.

ICAM-1 expression The two monoclonal antibodies to ICAM-1 (RR1/1

and BBA3) yielded identical immunostaining patterns with skeletal muscle. The vascular endothelial cells of all cases expressed ICAM-1, as did the infiltrating inflammatory cells of the patients with primary and secondary inflammation. While ICAM-1 expression by vascular endothelial cells was detected in most capillaries of inflammatory myopathy patients, it was weakly expressed by some vascular endotheliall cells of individuals with non inflammatory myopathy and normal controls. In the specimens with evidence of perifascicular atrophy, there was the tendency for ICAM-1 to be more intensely expressed by the vascular endothelial cells that were in or near the region of the atrophy. The muscle fibers of normal subjects and of individuals with neuropathic diseases did not express ICAC-I. By contrast, ICAM-1-positive muscle fibers were detected in 18 of the 38 cases of inflammatory myopathy. Their distribution was as follows : DM, 2/12 ; PM, 12/22; IBM, 2/2 ; sarcoid myopathy, 2/2. Positively stained muscle fibers were also found in 1/ 8 cases of DMD and 1/3 cases of myotonic dystrophy. In the latter two conditions, ICAM-1 expression was limited to the cytoplasm of some, but not all, small regenerating muscle fibers, but it was not detected in undamaged muscle fibers (Table 1). By contrast, ICAM-1 was detected in the cytoplasm of regenerating fibers of 12/38 inflammatory myopathy cases, as well as

J. Shimizu et al. : Sarcolemmal ICAM-I and HLA-DR 151

perimysium

Table 1. ICAM-I, HLA-ABC, HLA-DR expression in inflammatory myopathy. SCORING scale : -absent or sparse ; + small amount ; moderate amount ; 4t ; large amount.

endomysium

Case

+ -

-

-

+ + + + + + -t + + + it + + it + + +-it + it it it it +-it + + + + it it--+ it

1 immunoreactions in sarcolemma Pathological findings of undamaged muscle fibers

-

-

-

-

-

-

-

-

-

-

-

-

+ + + + + + -t +-it + i t it it it it it it--+ it-* it--+ it-# -+ -+ -+

Case No 1 I Skin 1 Biopsied Age’Sex change muscle

Polymyositis 1 2 3 4 5 6 7 8 9 10 1 1 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

or Dermatomyositis (PM, DM) 61 M -. biceps 62 M + deltoid 49 F + quad 41 F + biceps 57 F - biceps 52 F + deltoid 42 F + quad 13 M + deltoid 55 F - quad 42 M + biceps 45 F + deltoid 67 F + gastro 58 M - quad 61 M - quad 53 F + biceps 50 M - quad 50 F - quad 40 F - biceps 61 M - tibialis 75 F - biceps 67 F - biceps 43 F - deltoid 63 M - quad 44 F - biceps 32 F - deltoid 72 M - biceps 43 F + deltoid 56 F - biceps 78 F - quad 55 F - quad 59 F - biceps 68 F - biceps 46 F - quad 50 F + quad

Inclusion body myositis 1 74 F I 2 1 79F

Sarcoidosis 1 60 F 2 62 F

tibialis gastro

PFA

+ + + -

+ +

n = 3 n = 8 n = 3 n = 3 n = 2

inflammatory cell response

+-it I it-* +-it it--+

I

it-* 1 it-* +-it i t

ICAM-1

- -

+ + + + + + + + + + + + + +

+ + + +

HLA-ABC

-

+ + + + + -t + + + + -t + + + + + -t + + + + -t + -t -t + + + + + + + +

+ +

+ +

HLA-DR

+ + + + + +

+

+ + + +

P F A ; perifascicular atrophy


Fig. 1 ICAM- 1 immunoreactivity in skeletal muscle. Snap-frozen sections were used. Antibody binding was visualized by the avidin-biotin-immunoperoxidase complex (ABC) procedure. a : Reaction product deposits are seen in the sarcolemma (arrows), mononuclear cells and capillaries (double arrows) of a polymyositis patients (case 28). b, c and d : ICAM-I immunoreactivity is localized to capillaries of a normal control, an alcoholic neuropathy patient and a Duchenne muscular dystrophy patient, respectively.

X 350

X 270

in the sarcolemma of certain undamaged muscle fibers of 18 of the 38 cases (Fig. l a -d ; Fig.2a and b). Moreover, ICAM-1 expression was evident in the sarcolemma of some undamaged fibers of the PM and DM patients who had abundant endomysial inflammatory cells (Table 1). The sarcolemmal immunostaining observed in inflammatory myopathy was stronger in muscle fibers that were in the vicinity of endomysial inflammatory cells, with the staining pattern varying from focal to homogenous, depending on the distribution and the number of inflammatory cells.

HLA-ABC expression HLA-ABC expression was observed in vascular

endothelial cells, irrespective of disease, but not in normal skeletal muscle fibers. HLA-ABC-positive muscle fibers were detected in specimens from 37 cases

of inflammatory myopathy (DM : 12/12 ; PM : 21/ 22; IBM 2/2; sarcoid myopathy: 2/2), six of the 8 DMD patients, all three cases of myotonic dystrophy, and two cases of neuropathic diseases (alcoholic neuropathy: 1/3; M N D : 1/2). All, but one case of inflammatory myopathy showed strong, uniform HLA- ABC immunoreactivity in the sarcolemma of all muscle fibers. Sarcolemmal HLA-ABC immunostaining was not limited to the focal areas of cellular infiltration, and in some patients (cases 2, 3 and 4), intense reaction product deposits were seen in sections with no inflammatory cells (Table 1). Although HLA-ABC immunoreactivity was also evident in the sarcolemma of undamaged muscle fibers of 6/8 patients with DMD and all three myotonic dystrophy cases (Table l), staining was not uniform, as some fibers were not stained at all, while others had traces or

J. Shimizu et al. : Sarcolemmal ICAM-1 and HLA-DR 153

Fig. 2 a : ICAM-1 immunoreactivity (ABC method) and b : myosin ATPase activity (reaction at pH 4.3) in two consecutive sections from a patient with polymyositis (case 31). Asterisks in b denote type 2c fibers stained for residual myosin ATPase. As shown in a, the cytoplasm of these regenerating muscle fibers is immunostained by the anti-ICAM-1 antibody. X300

weak deposits of reaction products. In the positive samples from the patient with alcoholic polyneuropathy and that with MND, some of the small angulated fibers displayed weak sarcolemmal and sarcoplasmic HLA-ABC immunoreactivity. Moreover, certain small regenerating muscle fibers, irrespective of disease, showed weak sarcoplasmic immunostaining for HLA- ABC.

HLA-DR expression HLA-DR expression was seen in vascular endoth-

elial cells, irrespective of disease. Both anti-HLA-DR antibodies (LN3 and L243) used, gave identical results with respect to skeletal muscle; no normal muscle fiber expressed HLA-DR. Positively immunostained muscle fibers were detected in specimens from 18/38 cases of inflammatory myopathy (PM : 12/22 ; DM : 2/12 ; IBM : 2/2 ; sarcoid myopathy : 2/2), 2/8 cases of DMD, and 1/3 cases of myotonic dystrophy. Sarco- lemma1 HLA-DR expression was observed in un-

damaged muscle fibers of the 18 inflammatory myopathy cases who had large amounts of endomysial inflammatory cells (Table l), with staining being stronger in areas close to these cells. In addition, sarcolem- ma1 staining was also detected near the endomysial inflammatory cells in the two positive DMD cases and the patient with myotonic dystrophy. However, staining was weak in these cases and not as uniform as that seen in inflammatory myopathy. Moreover, certain small regenerating muscle fibers in the biopsy specimens of patients with inflammatory myopathy exhibit- ed diffuse sarcoplasmic immunostaining for HLA-DR.

Of the 34 cases of inflammatory myopathy examined, 19 (cases 2 to 20) revealed strongly positive staining for sarcolemmal HLA-ABC with no concomitant staining for either ICAM-1 or HLA-DR (Table 1 and Fig. 3a- c). By contrast, in 14 cases who had massive amounts of inflammatory cells (cases 21 to 34), HLA-DR and ICAM-1 were generally colocalized in the sarcolemma of the same fibers and in the vicinity of the inflammation (Fig. 3d-f).

Discussion

Our results demonstrate that muscle fibers in normal or neuropathic skeletal muscle specimens do not express ICAM- 1. Although sarcoplasmic ICAM-1 expression was seen in some regenerating fibers, irrespective of disease status, sarcolemmal expression in undamaged muscle fibers was specific for inflammatory myopathy. Autoimmune mechanisms are known to be important in the pathogenesis of PM, DM, sarcoidosis and IBM, with recognition of muscle fibers by infiltrating cells being essential. ICAM-I is a cell adhesion molecule that plays a cardinal role in the reaction between inflammatory and target cells. Hence, our demonstration of specific sarcolemmal ICAM- 1 expression in apparently undamaged muscle fibers from patients with inflammatory myopathy sug- gests that this molecule is important for the pathogenesis of the disease. It is conceivable that the presence of ICAM-1 may lead to activation of T lymphocytes, thereby triggering the ensuing tissue damage. There are precedents for this notion, since similar results have been described in other types of autoimmune disorders involving the thyroid50, Skin17,28,31,45 , k' idney9, as well as in rejected allograft tissues1.6. 12,30

The expression of HLA-ABC and HLA-DR in various muscle specimens, including those from patients with inflammatory myopathy patients, has been described before13.18~19~21~zg,53. However, although the HLA-ABC antigen has been detected in muscle


Fig. 3 Immunostaining for ICAM-I (a, d), HLA-ABC (b, c) and HLA-DR (c, f) in consecutive sections (snap frozen) from two dermatomyositis patients. Sections from an individual with few perimysial inflammatory cells (case 12) are shown in a-c, and those from a patient with perifascicular atrophy and endomysial infiltration of inflammatory cells (case 33), in d-f. Binding of primary antibodies detected by the ABC method. Sarcolemmal HLA-ABC immunoreactivity is seen in both cases (b and e), while expression of ICAM-1 and HLA-DR is evident only in the patient with inflammatory cells (d and f). Note parallel ICAM-I and HLA-DR immunostaining patterns.

J. Shirnizu et al. : Sarcolemmal ICAM-1 and HLA-DR 155

fibers of inflammatory myopathy patients, the expression of HLA-DR in muscle fibers from individuals with inflammatory disease is controversial. Thus, while some studies have shown its presence in the sarcolemma of muscle fibers in inflammatory myopa- thy32,37,53, others have reported that these fibers are devoid of HLA-DR21,29. These discrepancies may be due to the fact that different monoclonal antibodies were used in those studies.

The HLA-DR molecule consists of a light, 28 kD polypeptide chain noncovalently linked to a heavy, 33 kD polypeptide chain. Although a number of monoclonal antibodies to HLA-DR have been generated, they recognize different e p i t o p e ~ ~ ~ , ~ ~ - ~ ~ . Thus, whereas some antibodies react with epitopes on a single polypeptide chain, others recognize the structure of both chains. We used the monoclonal antibody L234, which recognizes the light plus heavy chain of the HLA-DR structure, and does not cross-react with HLA-DQ or HLA-DRs,35,39,40. It should be noted in the present context that our findings corroborate those of Olssen et al., who employed the same antibody to demonstrate HLA-DR expression in the sarcolemma of muscle fibers from patients with inflammatory r n y ~ p a t h y ~ ~ . Moreover, L243 has also been used for the immunohistochemical documentation of aberrant HLA-DR expression in cultured muscle cells15Jo, tissues from patients with other types of autoimmune disease^^^.^^, and rejected tissue allograft^^*^^.

We detected sarcolemmal HLA-ABC expression in undamaged muscle fibers of most cases of inflammatory myopathy. This expression did not correlate with the presence of inflammatory cells, nor with HLA-DR and/or ICAM-I expression. On the other hand, sarcolemmal expression of ICAM-1 and HLA-DR was evident in the cases with many endomysial inflammatory cells, and was strongest in the muscle fibers that were in the vicinity of these cells. Moreover, by using serial sections we were able to show that ICAM-1 and HLA-DR were colocalized in the same fibers. Although it has been suggested on the basis of immunohistochemical analysis of invading mononuclear cells that different immunological mechanisms are involved in the various types of inflammatory myopathies, including PM and DM2, our study demonstrates the colocalization of ICAM-1 and HLA- DR in specimens with massive endomysial inflammation. These observations were independent of the clinical diagnosis of the cases examined. These findings suggest that ICAM-1 and HLA-DR colocalization in undamaged muscle fibers correlates with the extent of the endomysial inflammatory response in patients with inflammatory myopathy.

It is known that several humoral factors can induce target cells to express ICAM-146,51, HLA-ABC13s47 or HLA-DR34. Our finding on differences in the expression patterns of these molecules by undamaged muscle fibers of patients with inflammatory myopathy would suggest dissimilarities with respect to the mechanisms involved in their induction in inflammatory disease processes. It is of significant interest that in the PM and DM patients who had few inflammatory cells, sarcolemmal HLA-ABC expression preceded immune cell infiltration. This would indicate that certain humoral factors may act as HLA-ABC inducers. On the other hand, in cases with massive endomysial inflammation, commmon factors such as local produc- tion of cytokines (e.g., interferon- y, tumor necrosis factor-a, interleukin-1) by inflammatory cells or inflammatory mediators released during ischemic stress may induce muscle fibers to express both, ICAM-1 and HLA-DR9J1J2. It should be noted in this context that HLA-DR induction by interferon-y has been described with cultured muscle cell^^^^^^. Thus, interferon-y may indeed be the factor that enables muscle fibers of PM and DM patients to express HLA-DR and ICAM- 1 concurrently.

Moreover, it has been shown that, in addition to cell-cell interactions mediated by CD8 and CD4 and their respective ligands HLA-ABC and HLA-DR, the interaction between LFA- 1 on lymphocytes and ICAM-1 on target cells is essential for the recognition of the latter by lymphocyte^^^^^^,^^^^^. Hence, the colocalization of ICAM-1 and HLA-DR in the sarcolemma of the same fiber may be important for the recognition of target cells by CD4-bearing lymphocytes, and the immunohistochemical changes may be important in recognition of target cells by lymphocytes or phagocytes, as well as in cell mediated cytotoxicity in autoimmune diseases. Basis for this notion is the aberrant co-expression of ICAM-I and HLA-DR in the same tissues, demonstrated in various autoimmune diseases9~26*42~45, and in rejected tissue allograft^^.^^.

The recent report by Bartoccioni et af .4 on HLA- ABC, HLA-DR and ICAM-1 expression in inflammatory myopathy is pertinent to the present results. These authors examined specimens from 18 patients with inflammatory myopathy, one with myasthenia gravis, and eight adult controls, and found HLA-ABC expression in muscle fibers from all inflammatory myopathy cases, and ICAM-1 expression in the specimens with widespread mononuclear infiltration. Bar- toccioni et af .4 also showed that in patients with inflammatory myopathy, some undamaged fibers near the infiltrating cells expressed both, ICAM-1 and

I56 Neuropathology 14, 1994

HLA-DR. Consequently, the results reported here are rather similar to these observations. From the data obtained in studying the 16 pathological control cases, we are able to conclude that sarcolemmal ICAM-1 expression on undamaged muscle fibers, and its colocalization with HLA-DR are indeed specific for inflammatory myopathy.

The recent demonstration that cultured myoblasts express ICAM-1 upon induction by inflammatory cytokines such as interferon-y and tumor necrosis factor- a5,I5 is of relevance with regard to the observed sarcoplasmic expression of ICAM-1 by certain regenerating fibers. ICAM-1 positive regenerating fibers were observed in specimens not only from PM or DM patients but also from a few cases of other myopathies. These findings would suggest that this intercellular adhesion molecule may also play a cardinal role in muscle fiber regeneration. However, since not all regenerating fibers expressed ICAM-1, it would appear that ICAM- 1 may be transiently induced during muscle fiber regeneration.

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Correspondence : Mitsuru Kawai, M.D., Department of Neurology, Shimoshizu National Hospital, Yotsukaido, Chiba, Japan

sarcolemmal coexpression of intercellular adhesion molecule-1 (icam-1) and hla-dr in inflammatory...

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