Transcriptomics and Genomics in Prostate Cancer

Prof. Dr. Guido Jenster Experimental Urological Oncology Erasmus MC Rotterdam [email protected] Basic Research: The prostate cancer problem Transcriptomics and genomics of prostate cancer

- What is the PCa problem and how to address it?

- DNA sequencing - Common, rare and private mutations - Personalized Medicine - Metastasis

- RNA sequencing - Small RNAs - Long RNAs

- Liquid biopsies

The prostate cancer problem

How to address the prostate cancer problem:

Early detection and cure via Hormone-, chemo-, immuno- Prevention surgery/radiation therapy therapy

Bone metastasis

Functional: Markers: Therapy targets: Understanding the -cancer risk? -which new medicines? components and -cancer present? -which order and combination? processes responsible -treatment needed? -therapy resistance? for cancer development -which treatment? and progression -treatment successful?

Markers and therapy targets for prostate cancer

Markers and therapy targets: An inventory of the differences between normal and cancer cells: Fusion DNA mutations Novel RNAs RNA Small RNAs

PCa nanobodies Androgen receptor

Metabolites Hormones Fatty acids

Morphology Exosomes Cellular behavior Pathology / Imaging Genes and pathways responsible for prostate cancer initiation and progression

TMPRSS2-ERG fusion

PTEN inactivation

Myc overexpression P53 AR inactivation amplification DNAseq Data Analysis

Copy Number SNVs / InDels Abberations

TF Binding B-Allele Frequency

DNAseq data

Chromatin Interactions Structural Variations

Methylation Active Chromatin

Identify Read Integration Sites Barcode PCa genomics: The messy genome

FISH : painting

In the messy cancer genomes, the secret of the tumor characteristics are hidden

Van Bokhoven et al., The Prostate 57: 226-244 (2003) PCa genomics: The messy genome

The Molecular Taxonomy of Primary Prostate Cancer

How does this help an individual patient? TCGA, Cell 163, 4, 2015, Pages 1011–1025 PCa genomics: The messy genome

TCGA, Cell 163, 4, 2015, Pages 1011–1025

Actionable targets

PARP inhibitors Mateo et al., N Engl J Med. 2015 373(18):1697-708

PI3K and AKT inhibitors

Kinase inhibitors Markers and therapy-targets for prostate cancer How many changes are identified in the VCaP cell line?

On chromosome level: Breaks : 35

Base pair level: Breaks: 764 Small changes: 246,653

~ 10 common ~ 20 rare ~ 500 ~ 470 novel/private mutated

Teles Alves et al., Genetics (2013) Markers and therapy and Markers TMPRSS2

~50% Percentage tumors with gene change -ERG

Common

targets for for cancer -targets prostate targets therapy and markers logical most The ARHGEF3 THADA

The most common gene changesThegene most common Rare

Majority MAP4K3 LRBA

and RAF1 BRAF

newly

discovered GPS2

-MPP2 MPP5

Private

-FAM71D PRRT2

The prostate cancer problem

Personalized oncology / Precision medicine

Search for changes in the tumor (such as DNA) that indicate:

“Who should be treated when and with which medicines”

Tumor type determines choice and order of therapy

Type of DNA mutation and tumor type determine choice and order of therapy

However, for many (rare/private) mutations we have no medicine PCa genomics: The messy genome

The issue with heterogeneity and clonality Gundem et al., Nature 520: 353-357 (2015) PCa genomics: The messy genome

Will the Personalized Medicine approach cure these patients? Gundem et al., Nature 520: 353-357 (2015) PCa genomics: Heterogeneity, clonal origin and re-population

Cooper CS et al., Nat Genet. 2015 Apr;47(4):367-72.

Su F et al., Eur Urol. 2018 Jun 22. pii: S0302-2838(18)30430-5 ‘All’ tumors represented:

Biopsy Blood Urine

Identify trunk mutations

Primary tumor single cell sequencing Gundem et al., Nature 520: 353-357 (2015) PCa genomics: The messy genome

The Molecular Taxonomy of Primary Prostate Cancer

TCGA, Cell 163, 4, 2015, Pages 1011–1025 Basic Research: The prostate cancer problem Transcriptomics and genomics of prostate cancer

- What is the PCa problem and how to address it?

- DNA sequencing - Common, rare and private mutations - Personalized Medicine - Metastasis

- RNA sequencing - Small RNAs - Long RNAs

- Liquid biopsies

Which type of RNA is most abundant?

How many different genes do we have per type?

Table 6-1 Molecular Biology of the Cell (© Garland Science 2008) Transcriptomics of PCa tissue: discovery of novel PCa-associated transcripts

How many genes do have?

1) Up to 25,000

2) 25,000 – 60,000

3) 60,000 – 100,000

4) More than 100,000 RNAseq Data Analysis

sdRNAs; tRFs PCA3

RNA modification Differential expression

AR T877A ARv7

Alternative splicing & SNV / InDels RNAseq data Promoters

Read-Through & Novel Transcripts Fusion Transcripts

EPCAT176 (SChLAP1) TMPRSS2-ERG Small RNAs in prostate cancer progression Early detection and cure via Hormone-, chemo-, immuno- Prevention surgery/radiation therapy therapy

Bone metastasis

NAP: Normal Adjacent Prostate BPH: Benign Prostate Hyperplasia PCa: Organ-confined Prostate Cancer LN: PCa Lymph Node Metastases TURP-PCa: Castration Resistant PCa

RNA pools of 4 fresh frozen patient samples for each group - size fractionation 18-35 nt - adaptor ligation, cDNA amplification and Solexa/Illumina sequencing (30-35 bp) Inventory of small RNAs in prostate and PCa samples

Martens et al., Oncogene 2012;31(8):978-91. Families of small nucleolar RNA (snoRNA)

snoRNA H/ACA-box snoRNA C/D-box scaRNAs PseudoUridylation of rRNA Methylation of rRNA Modification of RNA N= ±120 N= ±260 N= ±25 SNORA SNORD H/ACA and C/D-box snRNA

Name Abbr. Function Size (nt) Post-transcriptional gene Micro RNA miRNA 21-24 regulation Small Nucleolar RNA snoRNA Modification of rRNAs 70-130 Small Cajal Body-specific RNAs scaRNA Modification of snRNAs 80-350 ?

Hypothesis: Not only pre-miRNAs, but also other ncRNAs are specifically processed to smaller (functional ?) fragments snoRNAs from the GAS5 locus are up-regulated in prostate cancer

GAS5 SNORDS NAP BPH PCa LN

SNORD81 233 157 1,024 1,905

SNORD47 4 7 76 94 SNORD80 9 4 5 22 SNORD79 28 40 200 359 SNORD78 545 168 2,469 10,658 SNORD44 2,396 3,111 11,391 11,117 SNORD77 SNORD76 SNORD75 36 88

Prostate Cancer SNORD74 853 645 3,235 5,166

GAS5 mRNA 20 20 31 45

From Exon Arrays

Normal adjacent prostate Martens-Uzunova ES et al., Oncotarget. 2015 Fragments generated from the GAS5 locus

05 32 07 300 08 404

11 117 11 846

800 325

800 405 Fragments generated from the GAS5 locus Basic Research: The prostate cancer problem Transcriptomics and genomics of prostate cancer

- What is the PCa problem and how to address it?

- DNA sequencing - Common, rare and private mutations - Personalized Medicine - Metastasis

- RNA sequencing - Small RNAs - Long RNAs

- Liquid biopsies

A novel EMC Prostate Cancer-Associated Transcript (EPCAT) A novel EMC Prostate Cancer-Associated Transcript (EPCAT)

Junction track Compilation of RNAseq reads

20 matched NAP

20 PCa

Gene Left Gene Left EPCAT966 Gene Right Transcriptomics of PCa tissue: validation of novel PCa-associated transcripts Novel genes: Erasmus MC Prostate Cancer-Associated Transcripts

EPCATs are long noncoding RNAs and not conserved Transcriptomics of PCa tissue: validation of novel PCa-associated transcripts

No PCa: n=117 + 74 (cystoprostatectomy / pelvic exenteration / TURP BPH)

Local PCa: n=481 Radical prostatectomy

LN metastases: n=119

TURP-PCa: n=120 (65 CRPC; 55 HS)

Böttcher R et al., Oncotarget. 2015 Feb 28;6(6):4036-50. Prostate Cancer Biomarkers: validation of novel PCa-associated transcripts PCa-associated transcripts (EPCATs) In situ hybridization EPCAT176 / SChLAP1 EPCAT176 overall survival

Böttcher R. et al., Oncotarget. 2015 28;6(6):4036-50. Prostate Cancer Biomarkers: novel transcripts Prostate Cancer Biomarkers: novel transcripts

Tissue-specific circRNAs

PCa cells tissue

Chen S, …Jenster G, ...Boutros P, He H, Cell in press Basic Research: The prostate cancer problem Transcriptomics and genomics of prostate cancer

- What is the PCa problem and how to address it?

- DNA sequencing - Common, rare and private mutations - Personalized Medicine - Metastasis

- RNA sequencing - Small RNAs - Long RNAs

- Liquid biopsies

Prostate Cancer Research: Liquid biopsy

CELL-FREE CIRCULATING TUMOR PROTEIN RNA CELLS

METABOLITES

CELL-FREE DNA

EXTRACELLULAR VESICLES (EV-RNA; EV- PROTEINS; EV-DNA)

PLATELETS

VIRUSES

MICRO- Urine ORGANISMS Serum Prostate Cancer Research: Liquid biopsy cell-free DNA

Targeted cfDNA mutational analysis (72 mCRPC genes) WGS cfDNA mutational analysis (low pass)

Wyatt AW et al., J Natl Cancer Inst. 2017 Dec 1;109(12) Viswanathan SR et al., Cell. 2018 Jul 12;174(2):433-447.e19 Diagnosis and prognosis of urogenital diseases

The URINOME Project

RNA and DNA from:

Kidney Bladder Prostate

Representing:

Infection Cancer Stones Chronic disease Congenital diseases Transplantation

Children, women and men ERG

RNAseq of urine: TMPRSS2-ERG fusion transcript detected in a man with PCa Markers and therapy and Markers TMPRSS2

~50% Percentage tumors with gene change Common -ERG

targets for for cancer -targets prostate Biomarkers/ PCATs AR AR circRNAs sdRNAs variants /PCA3 Targets

?

targets therapy and markers logical most The ARHGEF3 THADA

The most common gene changesThegene most common Rare

MAP4K3 LRBA

Newly discovered Newly

HES6 SKIL

GPS2

-MPP2 MPP5 Private

-FAM71D PRRT2