Cover/Title page

Supporting Information

Comparative Proteomic Profiling of Adrenocortical Neoplasia Using Mass Spectrometry

Jean Lucas Kremer1, Henrique Sanchez Ortega1, Talita Souza-Siqueira2, Claudia Blanes Angeli3, Leo Kei Iwai4, Claudimara Ferini Pacicco Lotfi1*

1. Institute of Biomedical Sciences, Department of Anatomy, University of São Paulo, São Paulo, Brazil, Av. Prof. Lineu Prestes, 2415, Butantan, São Paulo, SP, 05508-000.

2. School of Medicine, Department of Clinical Medicine, University of São Paulo, Brazil, Av. Dr. Arnaldo, 455, Cerqueira César, São Paulo, SP, 01246903.

3. Institute of Biomedical Sciences, Department of Parasitology, University of São Paulo, Brazil, Av. Prof. Lineu Prestes, 1374, Butantan, São Paulo, SP, 05508-000.

4. Butantan Institute, Laboratory of Applied Toxicology, Center of Toxins, Immune- response and Cell Signaling LETA/CeTICS Laboratory, Brazil, Av. Vital Brasil, 1500 - Butantã, São Paulo, SP, 05503-900.

*Corresponding author: clotfi@usp.br.

Table of Contents

Figure S1. The histopathological characteristics of A) normal human adrenal (NHA); B) adenoma adrenocortical (ACA); C) carcinoma adrenocortical; D) Primary macronodular hyperplasia adrenal (with mutation in the ARMC5 gene (PMAHw); E) Primary macronodular hyperplasia adrenal (without mutation in the ARMC5 gene (PMAHwt). Supplementary_File_Figure S1.pdf.

Figure S2. Correlation of proteomics-identified targets with clinical data in ACC using Gene Expression Profiling Interactive Analysis (GEPIA platform); Overall Survival (OS); disease-free survival (DFS). SRRM2 = serine/arginine repetitive matrix 2; NUP160 = nuclear pore complex protein; RBM3 = RNA-binding motif protein 3. Supplementary_File_Figure S2.pdf.

Figure S3. Differentially expressed protein of hyperplasia with and without ARMC5 mutation. A) The number of total proteins expressed in PMAHwt and PMAHw, the overlapping part of the circle indicates the number of proteins expressed in both groups; B) Heatmap of DEPs identified in PMAHw and PMAHwt; C) Volcano plots for significantly differentially expressed proteins PMAHwt vs. PMAHw. The -log10 (FDR) is plotted against log2 (Fold-Change). PMAHw = primary macronodular adrenal hyperplasia with ARMC5 mutation, PMAHwt = primary macronodular adrenal hyperplasia without ARMC5 mutation, DEPs = differentially expressed proteins, FDR = false discovery rate. Supplementary_File_Figure S3.pdf.

Figure S4. Biological processes identified by network enrichment analysis using Gene Ontology (GO) and STRING platforms of 64 adrenocortical carcinomas (ACC) upregulated proteins relative to adrenocortical adenomas (ACA). FDR = false discovery rate. Supplementary_File_Figure S4.pdf.

Figure S5. High expression of STMN1 and PHGDH is associated with aggressive behavior and poor patient outcomes in ACC, whereas NDRG4 expression is the opposite. Kaplan-Meier survival plot of overall survival (OS), disease-free survival (DFS), and expression across tumor stages of A) Stathmin 1 (STMN1); B) phosphoglycerate dehydrogenase (PHGDH); C) N-myc downregulated gene family 4 (NDRG4) expression from TCGA analysis. n = 38. Supplementary_File_Figure S5.pdf.

Table S1 - Total proteins identified in primary macronodular adrenocortical hyperplasia without ARMC5 mutation. Supplementary_File_Table S1.xlsx.

Table S2 - Total proteins quantified in all analyzed samples. Supplementary_File_Table S2.xlsx.

Table S3 - Proteins identified specifically in each group and Proteins exclusively identified comparing all groups. Supplementary_File_Table S3.xlsx.

Table S4 - Proteins identified as up- or downregulated between the two conditions. Supplementary_File_Table S4.xlsx.

Table S5 - Cross-validation of DEPs in ACC-SNUH identified in ACC-USP on comparison between the two conditions. Supplementary_File_Table S5.xlsx.

Figure S1. The histopathological characteristics of A) normal human adrenal (NHA); B) adenoma adrenocortical (ACA); C) carcinoma adrenocortical; D) Primary macronodular hyperplasia adrenal (with mutation in the ARMC5 gene (PMAHw); E) Primary macronodular hyperplasia adrenal (without mutation in the ARMC5 gene (PMAHwt). C = capsule; ZG = zone glomerulosa; ZF = zone fasciculada; ZR = zone reticular.

A

B

C

ZR

ZF

ZG

C

0.1 mm

0,1 mm

0.1 mm

D

E

0.0 mm

0.1 mm

SRRM2

Disease Free Survival

1.0

Low SRRM2 TPM

High SRRM2 TPM

Logrank p=0.026

0.8

HR(high)-2.1

p(HR)-0.031

Percent survival

n[high)-38

0.6

n(low)-38

0.4

0.2

0.0

0

50

100

150

Months

Overall Survival

1.0

Low SRRM2 TPM

High SRRM2 TPM

Logrank p=0.31

0.8

HR(high)=1.5

p(HR)-0.33

Percent survival

n(high)-38

0.6

n(low)-38

0.4

0.2

0.0

0

50

100

150

Months

Expression across tumor stages

:

F value = 2.14

Pr(>F) = 0.103

9

-

Stage I

Stage II

Stage III

Stage IV

NUP160

Overall Survival

1.0

Low NUP160 TPM

High NUP160 TPM

Logrank p=0.085

0.8

HR(high)-2

p(HR)-0.09

Percent survival

n(high)=38

0.6

n(low)-38

0.4

0.2

0.0

0

50

100

150

Months

Disease Free Survival

0

Low NUP160 TPM

High NUP160 TPM

Logrank p=0.0039

0.8

HR(high)=2.7

p(HR)-0.0058

Percent survival

n(high)-38

0.6

n(low)-38

0.4

0.2

0.0

0

50

100

150

Months

Expression across tumor stages

F value = 1.39

Pr(>F) = 0.254

+

(

2

-

Stage 1

Stage II

Stage III

Stage IV

RBM3

Disease Free Survival

1.0

Overall Survival

Low RBM3 TPM

High RBM3 TPM

1.0

Low RBM3 TPM

Logrank p=0.32

High RBM3 TPM

0.8

HR(high)-1.4

Logrank p=0.75

p(HR)-0.32

0.8

HR(high)-1.1

Percent survival

n(high)-38

p[HR)-0.76

n(low)-38

n[high)-38

0.6

Percent survival

0.6

n(low)-38

0.4

0.4

0.2

0,2

0.0

0.0

0

50

100

150

Months

0

50

100

150

Months

Expression across tumor stages

Figure S2. Correlation of proteomics-identified targets with clinical data in ACC using Gene Expression Profiling Interactive Analysis (GEPIA platform); Overall Survival (OS); disease-free survival (DFS). SRRM2 = serine/arginine repetitive matrix 2; NUP160 = nuclear pore complex protein; RBM3 = RNA binding motif protein 3.

=

F value = 0.656

Pr(>F) - 0.582

10

9

00

A

6

5

Stage I

Stage II

Stage III

Stage IV

A)

PMAHwt

PMAHw

717

4475

203

B)

PMAHW

PMAHW

PMAHW

PMAHW

PMAHW

PMAHwt

PMAHwt

PMAHwt

PMAHwt

PMAHwt

C)

PMAHwt_vs_PMAHw_DEPs.

NOSTRIN

PCP4

6

C4BPB

PSPH

AKAP7

SNU13

STAB1

POLR21

GPKOW

-log10(P-Value)

4

POLR2B

CES2

RNPS1

Regulation

RDH13

POTEJ

PNPT1

ACYP2

Downregulated

Not Significant

Upregulated

2

0

-1.0

-0.5

0.0

0.5

1.0

log2(Fold Change)

Figure S3. Differentially expressed protein of hyperplasia with and without ARMC5 mutation. A) The number of total proteins expressed in PMAHw and PMAHwt, the overlapping part of the circle indicates the number of proteins expressed in both groups; B) Heatmap of DEPs identified in PMAHw and PMAHwt; C) Volcano plots for significantly differentially expressed proteins PMAHw vs. PMAHwt. The -log10 (FDR) is plotted against log2 (Fold-Change). PMAHw = primary macronodular adrenal hyperplasia with ARMC5 mutation, PMAHwt = primary macronodular adrenal hyperplasia without ARMC5 mutation, DEPs = differentially expressed proteins, FDR = false discovery rate.

ACYP2

AKA7G

C4BPB

GPKOW NOSTN

PCP4

RPB2

RPB9

POTEJ

SERB

RNPS1 NH2L1

EST2

PNPT1

RDH13

STAB1

Biological Process (Gene Ontology) enrichment

FDR

Regulation of stem cell differentiation

3.4e-04

5.2e-04

Chromatin remodeling

7.7e-04

1.1e-03

Nu cleobase-containing compound metabolic process

1

1.7e-03

2.6e-03

Nucleic acid metabolic process

İ

Groups at similarity 0.8

Gene count

Cellular nitrogen compound metabolic

process

1

5

Macromolecule metabolic process

15

30

Nitrogen compound metabolic process

Organic substance metabolic process

40

Metabolic process

Primary metabolic process

0.30

0.35

0.40

0.45

0.50

0.55

0.60

0.65

Signal

Reactome Pathways enrichment

Figure S4. Biological processes identified by network enrichment analysis using Gene Ontology (GO) and STRING platforms of 64 adrenocortical carcinomas (ACC) upregulated proteins relative to adrenocortical adenomas (ACA). FDR = false discovery rate.

FDR

Positive epigenetic regulation of rRNA

2.0e-05

expression

1

5.8e-05

Processing of Capped Intron-Containing Pre-mRNA

1.6e-04

4.7e-04

Metabolism of RNA

1.3e-03

3.8e-03

mRNA Splicing - Major Pathway

Groups at similarity 0.8

Gene count

Late Phase of HIV Life Cycle

1

3

Regulation of TP53 Activity through Acetylation

☒ 6

Transport of the SLBP Dependant Mature mRNA

9

Transport of the SLBP independent Mature mRNA

12

Transport of Mature mRNA Derived from an Intronless Transcript

SUMOyla tion

0.5

0.6

0.7

0.8

0.9

1.0

1.1

Signal

STMN1

Overall Survival

Disease Free Survival

Expression across tumor stages

1.0

Low STMN1 TPM

High STMN1 TPM

0

Logrank p=1.4e-06

HR(high)=5.6

0.8

p(HR)=1.4e-05

n(high)=38

n(low)=38

0.6

CD

0.4

0.2

0.0

2

0

50

100

150

Months

F value = 8.64

Pr(>F) = 5.82e-05

Stage I

Stage II

Stage III

Stage IV

B)

PHGDH

Disease Free Survival

1.0

Low PHGDH TPM

High PHGDH TPM

Logrank p=0.0051

HR(high)=2.6

0.8

p(HR)=0.007

n(high)=38

n(low)-38

0.6

0.4

0.2

0.0

0

50

100

150

Months

Expression across tumor stages

F value = 9.34

00

Pr(>F) = 2.78e-05

6

+

2

.

0

Stage I

Stage II

Stage III

Stage IV

C)

NDRG4

Figure S5. High expression of STMN1 and PHGDH is associated with aggressive behavior and poor patient outcomes in ACC, whereas NDRG4 expression is the opposite. Kaplan-Meier survival plot of overall survival (OS), disease-free survival (DFS), and expression across tumor stages of A) Stathmin 1 (STMN1); B) phosphoglycerate dehydrogenase (PHGDH); C) N-myc downregulated gene family 4 (NDRG4) expression from TCGA analysis. n = 38.

Disease Free Survival

Overall Survival

Expression across tumor stages

1.0

Low NDRG4 TPM

1.0

High NDRG4 TPM

Low NDRG4 TPM

High NDRG4 TPM

F value = 4.23 Pr(>F) = 0.00822

Logrank p=0.0012

HR(high)=0.33

Logrank p=5.6e-07

0.8

p(HR)=0.0019

0.8

HR(high)=0.097

0

n(high)=38 n(low)=38

-P(HR) :- 3.2e-05

Percent survival

Percent survival

n(high)=38 n(low)=38

-

0.6

0.6

6

0.4

0.4

0.2

0.2

2

0.0

0.0

0

0

50

100

150

0

50

100

150

Stage I

Stage II

Stage III

Stage IV

Months

Months

1.0

Low STMN1 TPM

High STMN1 TPM

Logrank p=4.1e-06

0.8

HR(high)=7.3

p(HR)=7.2e-05

Percent survival

n(high)=38

0.6

n(low)=38

0.4

0.2

0.0

0

50

100

150

Months

Overall Survival

1.0

Low PHGDH TPM

High PHGDH TPM

Logrank p=0.0028

0.8

HR(high)=3.5

p(HR)=0.0047

Percent survival

n(high)=38

0.6

n(low)-38

0.4

0.2

0.0

0

50

100

150

Months

Percent survival

Percent survival